Unexpected Specificity of Interspecies Cobamide Transfer from Geobacter spp. to Organohalide-Respiring Dehalococcoides mccartyi Strains

Yan, Jun; Ritalahti, Kirsti M.; Wagner, Darlene; Löffler, Frank E.

doi:10.1128/aem.01535-12

Cited by 120 publications

(134 citation statements)

References 43 publications

(48 reference statements)

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“…Following autoclaving, the bottles were amended with 10 ml hydrogen and 25 mg l 21 CN-Cbl as described [15]. Neat TCE (5 ml, 99%, Fisher, Pittsburgh, PA, USA) and cis-DCE (5 ml, 99.5%, Sigma-Aldrich-Fluka, St Louis, MO, USA) were added with a microlitre syringe (Hamilton, Reno, NV, USA …”

Section: Methods (A) Pure Cultures and Growth Conditionsmentioning

confidence: 99%

“…were established in 160 ml vessels inside an anoxic chamber as described [15]. The vessels were amended with 5 mM acetate and contained a H 2 -CO 2 (80/20, v/v) headspace.…”

Section: (B) Co-culturesmentioning

confidence: 99%

“…Cells from Dehalococcoides pure cultures and co-cultures were harvested from 1 ml culture suspension as described [15,24]. Briefly, total genomic DNA was extracted using the MO BIO Soil DNA Isolation kit (MO BIO, Carlsbad, CA, USA), and a high efficiency bead ruptor homogenizer (Omni International, Kennesaw, GA, USA) following the manufacturer's protocols.…”

Section: (B) Co-culturesmentioning

confidence: 99%

“…Recently, interspecies cobalamin transfer from Geobacter lovleyi to D. mccartyi strains BAV1 and FL2 was demonstrated in CN-Cbl-free co-cultures [15]. Geobacter sulfurreducens did not support Dehalococcoides activity unless DMB was supplied to the growth medium suggesting that only the cobamides with specific types of lower ligands, such as DMB, meet Dehalococcoides' nutritional requirements.…”

Section: Introductionmentioning

confidence: 99%

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Guided cobalamin biosynthesis supports Dehalococcoides mccartyi reductive dechlorination activity

Yan

Yang

et al. 2013

Phil. Trans. R. Soc. B

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124

101

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Dehalococcoides mccartyi strains are corrinoid-auxotrophic Bacteria and axenic cultures that require vitamin B 12 (CN-Cbl) to conserve energy via organohalide respiration. Cultures of D. mccartyi strains BAV1, GT and FL2 grown with limiting amounts of 1 µg l −1 CN-Cbl quickly depleted CN-Cbl, and reductive dechlorination of polychlorinated ethenes was incomplete leading to vinyl chloride (VC) accumulation. In contrast, the same cultures amended with 25 µg l −1 CN-Cbl exhibited up to 2.3-fold higher dechlorination rates, 2.8–9.1-fold increased growth yields, and completely consumed growth-supporting chlorinated ethenes. To explore whether known cobamide-producing microbes supply Dehalococcoides with the required corrinoid cofactor, co-culture experiments were performed with the methanogen Methanosarcina barkeri strain Fusaro and two acetogens, Sporomusa ovata and Sporomusa sp. strain KB-1, as Dehalococcoides partner populations. During growth with H 2 /CO 2 , M. barkeri axenic cultures produced 4.2 ± 0.1 µg l −1 extracellular cobamide (factor III), whereas the Sporomusa cultures produced phenolyl- and p -cresolyl-cobamides. Neither factor III nor the phenolic cobamides supported Dehalococcoides reductive dechlorination activity suggesting that M. barkeri and the Sporomusa sp. cannot fulfil Dehalococcoides ' nutritional requirements. Dehalococcoides dechlorination activity and growth occurred in M. barkeri and Sporomusa sp. co-cultures amended with 10 µM 5′,6′-dimethylbenzimidazole (DMB), indicating that a cobalamin is a preferred corrinoid cofactor of strains BAV1, GT and FL2 when grown with chlorinated ethenes as electron acceptors. Even though the methanogen and acetogen populations tested did not produce cobalamin, the addition of DMB enabled guided biosynthesis and generated a cobalamin that supported Dehalococcoides ' activity and growth. Guided cobalamin biosynthesis may offer opportunities to sustain and enhance Dehalococcoides activity in contaminated subsurface environments.

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Section: Methods (A) Pure Cultures and Growth Conditionsmentioning

confidence: 99%

“…were established in 160 ml vessels inside an anoxic chamber as described [15]. The vessels were amended with 5 mM acetate and contained a H 2 -CO 2 (80/20, v/v) headspace.…”

Section: (B) Co-culturesmentioning

confidence: 99%

Section: (B) Co-culturesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Guided cobalamin biosynthesis supports Dehalococcoides mccartyi reductive dechlorination activity

Yan

Yang

et al. 2013

Phil. Trans. R. Soc. B

Self Cite

124

101

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“…Six chlorophenol and four PCE/trichloroethene (TCE) reductive dehalogenases have been purified from different Desulfitobacterium strains, and the majority of reductive dehalogenases that have so far been tested for the presence of a corrinoid prosthetic group contained such a group [49]. These corrinoid co-factors are thought to be essential for enzymatic function, and show some specificity: cocultures of Geobacter strains and Dehalococcoides mccartyi strains revealed cobamides produced by the OHRB Geobacter lovleyi strain SZ supported dechlorination by the Dehalococcoides strain, while cobamides produced by the non-OHRB Geobacter sulfurreducens did not [50].…”

Section: Reductive Dehalogenasesmentioning

confidence: 99%

Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases

Hug

Maphosa

Leys

et al. 2013

Phil. Trans. R. Soc. B

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266

277

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Organohalide respiration is an anaerobic bacterial respiratory process that uses halogenated hydrocarbons as terminal electron acceptors during electron transport-based energy conservation. This dechlorination process has triggered considerable interest for detoxification of anthropogenic groundwater contaminants. Organohalide-respiring bacteria have been identified from multiple bacterial phyla, and can be categorized as obligate and non-obligate organohalide respirers. The majority of the currently known organohalide-respiring bacteria carry multiple reductive dehalogenase genes. Analysis of a curated set of reductive dehalogenases reveals that sequence similarity and substrate specificity are generally not correlated, making functional prediction from sequence information difficult. In this article, an orthologue-based classification system for the reductive dehalogenases is proposed to aid integration of new sequencing data and to unify terminology.

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Coupling dark metabolism to electricity generation using photosynthetic cocultures

Badalamenti

Torres

Krajmalnik‐Brown

2013

Biotech & Bioengineering

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We investigated the role of green sulfur bacteria inlight-responsive electricity generation in microbial electrochemical cells (MXCs). We operated MXCs containing either monocultures or defined cocultures of previously enriched phototrophic Chlorobium and anode-respiring Geobacter under anaerobic conditions in the absence of electron donor. Monoculture control MXCs containing Geobacter or Chlorobium neither responded to light nor produced current, respectively. Instead, light-responsive current generation occurred only in coculture MXCs. Current increased above background levels only in the dark and declined slowly over 96 h. This pattern suggested that Chlorobium exhausted intracellular glycogen reserves via dark fermentation to supply an electron donor, presumably acetate, to Geobacter. With medium containing sulfide as the sole photosynthetic electron donor, current generation had a similar and reproducible negative light response. To investigate whether this metabolic interaction also occurred without an electrode, we performed coculture experiments in batch serum bottles. In this setup, sulfide served as the sole electron donor, whose oxidation by Chlorobium was required to provide S(0) as the electron acceptor to Geobacter. Copies of Geobacter 16S rDNA increased approximately 14-fold in batch bottle cocultures containing sulfide compared to those lacking sulfide, and did not decline after termination of sulfide feeding. These results suggest that products of both photosynthesis and dark fermentation by Chlorobium were sufficient both to yield an electrochemical response by Geobacter biofilms, and to promote Geobacter growthin batch cocultures. Our work expands upon the fusion of MXCs with coculture techniques and reinforces the utility of microbial electrochemistry for sensitive, real-time monitoring of microbial interactions in which a metabolic intermediate can be converted to electrical current.

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Unexpected Specificity of Interspecies Cobamide Transfer from Geobacter spp. to Organohalide-Respiring Dehalococcoides mccartyi Strains

Cited by 120 publications

References 43 publications

Guided cobalamin biosynthesis supports Dehalococcoides mccartyi reductive dechlorination activity

Guided cobalamin biosynthesis supports Dehalococcoides mccartyi reductive dechlorination activity

Overview of organohalide-respiring bacteria and a proposal for a classification system for reductive dehalogenases

Coupling dark metabolism to electricity generation using photosynthetic cocultures

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