Accelerated Degradation of Exogenous Indole by<i>Burkholderia</i><i>unamae</i>Strain CK43B Exposed to Pyrogallol-Type Polyphenols

Kim, Dongyeop; Rahman, M. A.; Sitepu, Irnayuli R.; Hashidoko, Yasuyuki

doi:10.1271/bbb.130282

Cited by 10 publications

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“…B. unamae strain CK43B was found to degrade indole under aerobic conditions when supplemented with gallic acid or pyrogallol (27), showing a similar cometabolic effect of indole degradation as in the case of strain O153. Importantly, indoxyl was detected as the reaction intermediate as well as compounds of the ␤-ketoadipate pathway, anthranilic acid, and catechol, signifying the possible relationship between Iif proteins and indole biodegradation in the genus Burkholderia.…”

Section: Discussionmentioning

confidence: 64%

“…A number of indole-degrading bacterial microorganisms (26)(27)(28) as well as bacterial consortia (29) were reported previously, but no genetic background in these reports has been specified. Several possible intermediates in bacterial indole degradation are also known, but proteins with specific enzyme activities that drive the degradation cascade have not been identified in this context.…”

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confidence: 99%

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Indole Biodegradation in Acinetobacter sp. Strain O153: Genetic and Biochemical Characterization

Sadauskas

Vaitekūnas

Gasparavičiūtė

et al. 2017

Appl Environ Microbiol

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Indole is a molecule of considerable biochemical significance, acting as both an interspecies signal molecule and a building block of biological elements. Bacterial indole degradation has been demonstrated for a number of cases; however, very little is known about genes and proteins involved in this process. This study reports the cloning and initial functional characterization of genes (iif and ant cluster) responsible for indole biodegradation in Acinetobacter sp. strain O153. The catabolic cascade was reconstituted in vitro with recombinant proteins, and each protein was assigned an enzymatic function. Degradation starts with oxidation, mediated by the IifC and IifD flavin-dependent two-component oxygenase system. Formation of indigo is prevented by IifB, and the final product, anthranilic acid, is formed by IifA, an enzyme which is both structurally and functionally comparable to cofactor-independent oxygenases. Moreover, the iif cluster was identified in the genomes of a wide range of bacteria, suggesting the potential of widespread Iifmediated indole degradation. This work provides novel insights into the genetic background of microbial indole biodegradation.IMPORTANCE The key finding of this research is identification of the genes responsible for microbial biodegradation of indole, a toxic N-heterocyclic compound. A large amount of indole is present in urban wastewater and sewage sludge, creating a demand for an efficient and eco-friendly means to eliminate this pollutant. A common strategy of oxidizing indole to indigo has the major drawback of producing insoluble material. Genes and proteins of Acinetobacter sp. strain O153 (DSM 103907) reported here pave the way for effective and indigo-free indole removal. In addition, this work suggests possible novel means of indole-mediated bacterial interactions and provides the basis for future research on indole metabolism. KEYWORDS indole, biodegradation, bacterial metabolism, Acinetobacter, bacterial signaling, cofactor-independent oxygenases I ndole is an N-heterocyclic aromatic compound derived mainly by TnaA tryptophanase from L-tryptophan in Escherichia coli (1) and is widely found in natural environments. Indole acts as cell-to-cell signaling molecule that regulates the expression of several virulence genes (2-4), promotes biofilm formation (5-7), and mediates complex predator-prey interactions (8, 9). At high concentrations, indole and its derivatives exhibit toxic activity to both prokaryotic cells and animals and are even considered mutagens (10). Toxic indole concentrations reportedly vary for different microorganisms in the range of 0.5 to 5 mM (11). The main mechanisms of indole toxicity are reported to be an alteration of membrane potential with subsequent inhibition of cell division (12), depletion of ATP levels (13), and an inhibition of acyl-homoserine lactone (AHL)-based quorum sensing by regulator misfolding (14).In order to utilize aromatic compounds as an energy source, microorganisms have

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Section: Discussionmentioning

confidence: 64%

mentioning

confidence: 99%

Indole Biodegradation in Acinetobacter sp. Strain O153: Genetic and Biochemical Characterization

Sadauskas

Vaitekūnas

Gasparavičiūtė

et al. 2017

Appl Environ Microbiol

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“…strain [25] use indole as a growth substrate. While, Pseudomonas indoloxidans, P. aeruginosa [7], A. tumefaciens [10], and Burkholderia unamae strain CK43-B [26] can degrade indole without utilizing it as the sole carbon source. D. indolicum is the only anaerobic isolate identified to date that can utilize indole as a carbon and electron donor [27].…”

Section: Discussionmentioning

confidence: 99%

Isolation of Indole Utilizing Bacteria Arthrobacter sp. and Alcaligenes sp. From Livestock Waste

et al. 2016

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Indole is an interspecies and interkingdom signaling molecule widespread in different environmental compartment. Although multifaceted roles of indole in different biological systems have been established, little information is available on the microbial utilization of indole in the context of combating odor emissions from different types of waste. The present study was aimed at identifying novel bacteria capable of utilizing indole as the sole carbon and energy source. From the selective enrichment of swine waste and cattle feces, we identified Gram-positive and Gramnegative bacteria belonging to the genera Arthrobacter and Alcaligenes. Bacteria belonging to the genus Alcaligenes showed higher rates of indole utilization than Arthrobacter. Indole at 1.0 mM for growth was completely utilized by Alcaligenes sp. in 16 h. Both strains produced two intermediates, anthranilic acid and isatin, during aerobic indole metabolism. These isolates were also able to grow on several indole derivatives. Interestingly, an adaptive response in terms of a decrease in cell size was observed in both strains in the presence of indole. The present study will help to explain the degradation of indole by different bacteria and also the pathways through which it is catabolized. Furthermore, these novel bacterial isolates could be potentially useful for the in situ attenuation of odorant indole and its derivatives emitted from different types of livestock waste.

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“…150 mg) was extracted with EtOAc from the resulting culture fluid. Using a half of the mixture (74 mg), the target compound, also predominantly yielded in the static cultured medium, was purified by silica gel column chromatography and preparative TLC as we described earlier (19 …”

Section: Methodsmentioning

confidence: 99%

“…Also, we recently reported a cometabolic effect of gallic acid and some other pyrogallol-type polyphenols on aerobic indole degradation by Burkholderia unamae (19). Conversely, gallic acid suppressed indole degradation by static-cultured B. unamae CK43B.…”

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confidence: 94%

Induction of Biofilm Formation in the Betaproteobacterium Burkholderia unamae CK43B Exposed to Exogenous Indole and Gallic Acid

Kim

Sitepu

Hashidoko

2013

Appl Environ Microbiol

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bBurkholderia unamae CK43B, a member of the Betaproteobacteria that was isolated from the rhizosphere of a Shorea balangeran sapling in a tropical peat swamp forest, produces neither indole nor extracellular polymeric substances associated with biofilm formation. When cultured in a modified Winogradsky's medium supplemented with up to 1.7 mM indole, B. unamae CK43B maintains its planktonic state by cell swelling and effectively degrades exogenous indole. However, in medium supplemented with 1.7 mM exogenous indole and 1.0 mM gallic acid, B. unamae CK43B produced extracellular polymeric substances and formed a biofilm. The concentration indicated above of gallic acid alone had no effect on either the growth or the differentiation of B. unamae CK43B cells above a certain concentration threshold, whereas it inhibited indole degradation by B. unamae CK43B to 3-hydroxyindoxyl. In addition, coculture of B. unamae CK43B with indole-producing Escherichia coli in nutrient-rich Luria-Bertani medium supplemented with 1.0 mM gallic acid led to the formation of mixed cell aggregates. The viability and active growth of B. unamae CK43B cells in a coculture system with Escherichia coli were evidenced by fluorescence in situ hybridization. Our data thus suggest that indole facilitates intergenus communication between indole-producing gammaproteobacteria and some indole-degrading bacteria, particularly in gallic acid-rich environments.

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Accelerated Degradation of Exogenous Indole byBurkholderiaunamaeStrain CK43B Exposed to Pyrogallol-Type Polyphenols

Cited by 10 publications

References 35 publications

Indole Biodegradation in Acinetobacter sp. Strain O153: Genetic and Biochemical Characterization

Indole Biodegradation in Acinetobacter sp. Strain O153: Genetic and Biochemical Characterization

Isolation of Indole Utilizing Bacteria Arthrobacter sp. and Alcaligenes sp. From Livestock Waste

Induction of Biofilm Formation in the Betaproteobacterium Burkholderia unamae CK43B Exposed to Exogenous Indole and Gallic Acid

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