Selective enrichment yields robust ethene-producing dechlorinating cultures from microcosms stalled at cis-dichloroethene

Anca Delgado, Dae Wook Kang, Katherine G. Nelson, Devyn Fajardo-Williams, Joseph F. Miceli, Hansa Magee, Sudeep C. Popat, Rosa Krajmalnik-Brown

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Dehalococcoides mccartyi strains are of particular importance for bioremediation due to their unique capability of transforming perchloroethene (PCE) and trichloroethene (TCE) to non-toxic ethene, through the intermediates cis-dichloroethene (cis-DCE) and vinyl chloride (VC). Despite the widespread environmental distribution of Dehalococcoides, biostimulation sometimes fails to promote dechlorination beyond cis-DCE. In our study, microcosms established with garden soil and mangrove sediment also stalled at cis-DCE, albeit Dehalococcoides mccartyi containing the reductive dehalogenase genes tceA, vcrA and bvcA were detected in the soil/sediment inocula. Reductive dechlorination was not promoted beyond cis-DCE, even after multiple biostimulation events with fermentable substrates and a lengthy incubation. However, transfers from microcosms stalled at cis-DCE yielded dechlorination to ethene with subsequent enrichment cultures containing up to 109 Dehalococcoides mccartyi cells mL-1. Proteobacterial classes which dominated the soil/sediment communities became undetectable in the enrichments, and methanogenic activity drastically decreased after the transfers. We hypothesized that biostimulation of Dehalococcoides in the cis-DCE-stalled microcosms was impeded by other microbes present at higher abundances than Dehalococcoides and utilizing terminal electron acceptors from the soil/sediment, hence, outcompeting Dehalococcoides for H2. In support of this hypothesis, we show that garden soil and mangrove sediment microcosms bioaugmented with their respective cultures containing Dehalococcoides in high abundance were able to compete for H2 for reductive dechlorination from one biostimulation event and produced ethene with no obvious stall. Overall, our results provide an alternate explanation to consolidate conflicting observations on the ubiquity of Dehalococcoides mccartyi and occasional stalling of dechlorination at cis-DCE; thus, bringing a new perspective to better assess biological potential of different environments and to understand microbial interactions governing bioremediation.

Original languageEnglish (US)
Article numbere100654
JournalPLoS One
Volume9
Issue number6
DOIs
StatePublished - Jun 20 2014

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Dehalococcoides
dechlorination
Dechlorination
ethylene
Sediments
Soil
Soils
sediments
Environmental Biodegradation
Bioremediation
bioremediation
soil
gardens
vinyl chloride
Microbial Interactions
Vinyl Chloride
Trichloroethylene
enrichment culture
inoculum
Genes

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Selective enrichment yields robust ethene-producing dechlorinating cultures from microcosms stalled at cis-dichloroethene. / Delgado, Anca; Kang, Dae Wook; Nelson, Katherine G.; Fajardo-Williams, Devyn; Miceli, Joseph F.; Magee, Hansa; Popat, Sudeep C.; Krajmalnik-Brown, Rosa.

In: PLoS One, Vol. 9, No. 6, e100654, 20.06.2014.

Research output: Contribution to journalArticle

Delgado, Anca ; Kang, Dae Wook ; Nelson, Katherine G. ; Fajardo-Williams, Devyn ; Miceli, Joseph F. ; Magee, Hansa ; Popat, Sudeep C. ; Krajmalnik-Brown, Rosa. / Selective enrichment yields robust ethene-producing dechlorinating cultures from microcosms stalled at cis-dichloroethene. In: PLoS One. 2014 ; Vol. 9, No. 6.
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abstract = "Dehalococcoides mccartyi strains are of particular importance for bioremediation due to their unique capability of transforming perchloroethene (PCE) and trichloroethene (TCE) to non-toxic ethene, through the intermediates cis-dichloroethene (cis-DCE) and vinyl chloride (VC). Despite the widespread environmental distribution of Dehalococcoides, biostimulation sometimes fails to promote dechlorination beyond cis-DCE. In our study, microcosms established with garden soil and mangrove sediment also stalled at cis-DCE, albeit Dehalococcoides mccartyi containing the reductive dehalogenase genes tceA, vcrA and bvcA were detected in the soil/sediment inocula. Reductive dechlorination was not promoted beyond cis-DCE, even after multiple biostimulation events with fermentable substrates and a lengthy incubation. However, transfers from microcosms stalled at cis-DCE yielded dechlorination to ethene with subsequent enrichment cultures containing up to 109 Dehalococcoides mccartyi cells mL-1. Proteobacterial classes which dominated the soil/sediment communities became undetectable in the enrichments, and methanogenic activity drastically decreased after the transfers. We hypothesized that biostimulation of Dehalococcoides in the cis-DCE-stalled microcosms was impeded by other microbes present at higher abundances than Dehalococcoides and utilizing terminal electron acceptors from the soil/sediment, hence, outcompeting Dehalococcoides for H2. In support of this hypothesis, we show that garden soil and mangrove sediment microcosms bioaugmented with their respective cultures containing Dehalococcoides in high abundance were able to compete for H2 for reductive dechlorination from one biostimulation event and produced ethene with no obvious stall. Overall, our results provide an alternate explanation to consolidate conflicting observations on the ubiquity of Dehalococcoides mccartyi and occasional stalling of dechlorination at cis-DCE; thus, bringing a new perspective to better assess biological potential of different environments and to understand microbial interactions governing bioremediation.",
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AU - Miceli, Joseph F.

AU - Magee, Hansa

AU - Popat, Sudeep C.

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