Genetics of Polycyclic Aromatic Hydrocarbon Metabolism in Diverse Aerobic Bacteria

Habe, Hiroshi; Omori, Toshio

doi:10.1271/bbb.67.225

Cited by 386 publications

(232 citation statements)

References 135 publications

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“…Organic pollutants are subjected to microbial biodegradation exemplified by monitored natural attenuation (Dojka et al, 1998;Stapleton et al, 1998;Gieg et al, 1999), and corresponding pathways have been depicted from bacterial strains (Cerniglia, 1992;Habe and Omori, 2003). Present knowledge about catabolic pathways is restricted to culturable strains constituting a great minority of the bacteria inhabiting soils and sediments.…”

Section: Introductionmentioning

confidence: 99%

High aromatic ring-cleavage diversity in birch rhizosphere: PAH treatment-specific changes of I.E.3 group extradiol dioxygenases and 16S rRNA bacterial communities in soil

Sipilä

Keskinen²,

Akerman³

et al. 2008

The ISME Journal

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Genes encoding key enzymes of catabolic pathways can be targeted by DNA fingerprinting to explore genetic degradation potential in pristine and polluted soils. We performed a greenhouse microcosm experiment to elucidate structural and functional bacterial diversity in polyaromatic hydrocarbon (PAH)-polluted soil and to test the suitability of birch (Betula pendula) for remediation. Degradation of PAHs was analysed by high-performance liquid chromatography, DNA isolated from soil amplified and fingerprinted by restriction fragment length polymorphism (RFLP) and terminal restriction fragment length polymorphism (T-RFLP). Bacterial 16S rRNA T-RFLP fingerprinting revealed a high structural bacterial diversity in soil where PAH amendment altered the general community structure as well as the rhizosphere community. Birch augmented extradiol dioxygenase diversity in rhizosphere showing a rhizosphere effect, and further pyrene was more efficiently degraded in planted pots. Degraders of aromatic compounds upon PAH amendment were shown by the changed extradiol ring-cleavage community structure in soil. The RFLP analysis grouped extradiol dioxygenase marker genes into 17 distinct operational taxonomic units displaying novel phylogenetic clusters of ring-cleavage dioxygenases representing putative catabolic pathways, and the peptide sequences contained conserved amino-acid signatures of extradiol dioxygenases. A branch of major environmental TS cluster was identified as being related to Parvibaculum lavantivorans ring-cleavage dioxygenase. The described structural and functional diversity demonstrated a complex interplay of bacteria in PAH pollution. The findings improve our understanding of rhizoremediation and unveil the extent of uncharacterized enzymes and may benefit bioremediation research by facilitating the development of molecular tools to detect and monitor populations involved in degradative processes.

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Section: Introductionmentioning

confidence: 99%

High aromatic ring-cleavage diversity in birch rhizosphere: PAH treatment-specific changes of I.E.3 group extradiol dioxygenases and 16S rRNA bacterial communities in soil

Sipilä

Keskinen²,

Akerman³

et al. 2008

The ISME Journal

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“…In recent years, the biodegradation of PAHs has received considerable attention and a variety of micro-organisms have been reported to play important roles in the process (Pothuluri & Cerniglia, 1994;Shuttleworth & Cerniglia, 1995;Kanaly & Harayama, 2000;Habe & Omori, 2003;Tortella et al, 2005). Bioremediation technologies have increasingly been proposed to decontaminate PAH-contaminated sites (Harayama, 1997;Samanta et al, 2002;Parrish et al, 2004;Vinas et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

A novel degradation pathway in the assimilation of phenanthrene by Staphylococcus sp. strain PN/Y via meta-cleavage of 2-hydroxy-1-naphthoic acid: formation of trans-2,3-dioxo-5-(2′-hydroxyphenyl)-pent-4-enoic acid

2007

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Staphylococcus sp. strain PN/Y, capable of utilizing phenanthrene as a sole source of carbon and energy, was isolated from petroleum-contaminated soil. In the degradation of phenanthrene by strain PN/Y, various metabolites, isolated and identified by a combination of chromatographic and spectrometric analyses, revealed a novel phenanthrene assimilation pathway involving 2-hydroxy-1-naphthoic acid. Metabolism of phenanthrene was initiated by the dioxygenation on the 1,2-position of phenanthrene followed by meta-cleavage of phenanthrene-1,2-diol, leading to 2-hydroxy-1-naphthoic acid, which was then processed via a novel meta-cleavage pathway, leading to the formation of trans-2,3-dioxo-5-(29-hydroxyphenyl)-pent-4-enoic acid and subsequently to salicylic acid. In the lower pathway, salicylic acid was transformed to catechol, which was then metabolized by catechol-2,3-dioxygenase to 2-hydroxymuconaldehyde acid, ultimately forming TCA cycle intermediates. The catabolic genes involved in phenanthrene degradation were found to be plasmid-encoded. This detailed study of polycyclic aromatic hydrocarbon (PAH) metabolism by a Gram-positive species involving a unique ring-cleavage dioxygenase in a novel phenanthrene degradation pathway provides a new insight into the microbial degradation of PAHs. INTRODUCTIONPolycyclic aromatic hydrocarbons (PAHs) constitute a group of priority environmental pollutants, which are ubiquitous contaminants in soils and sediments and are of environmental concern because of their toxic, mutagenic and/or carcinogenic effects (Mastrangelo et al., 1996;Marston et al., 2001;Xue & Warshawsky, 2005). In recent years, the biodegradation of PAHs has received considerable attention and a variety of micro-organisms have been reported to play important roles in the process (Pothuluri & Cerniglia, 1994;Shuttleworth & Cerniglia, 1995;Kanaly & Harayama, 2000;Habe & Omori, 2003;Tortella et al., 2005). Bioremediation technologies have increasingly been proposed to decontaminate PAH-contaminated sites (Harayama, 1997;Samanta et al., 2002;Parrish et al., 2004;Vinas et al., 2005).Phenanthrene, a PAH with three condensed rings fused in angular fashion, has a 'bay-region' and a 'K-region' and is often used as a model substrate for studies on the metabolism of carcinogenic PAHs. Over the last 60 years, a number of studies on phenanthrene degradation by several Gram-negative and Gram-positive bacterial species have been reported (Evans et al., 1965;Kiyohara et al., 1976Kiyohara et al., , 1982Kiyohara & Nagao, 1978;Barnsley, 1983;Gibson & Subramanian, 1984;Houghton & Shanley, 1994;Adachi et al., 1999;Samanta et al., 1999), where various pathways and metabolic diversity involved in phenanthrene degradation were documented. In general, the metabolic pathway is initiated by the double hydroxylation of the bay-region of phenanthrene by a dioxygenase enzyme to form cis-3,4-phenanthrenedihydrodiol. The resultant dihydrodiol is then converted by the action of dihydrodiol dehydrogenase to 3,4-dihydroxyphenanthrene, which und...

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“…Naphthalene, a polycyclic aromatic hydrocarbon (PAH) and constituent of coal tar, belongs to a class of widespread organic pollutants. Many bacterial species of Pseudomonas, Mycobacterium, Sphingomonas, Burkholderia and Ralstonia (Habe and Omori, 2003) degrade PAHs, and there is a substantial interest to optimize PAH bioremediation. However, biodegradation of PAHs in the environment is often limited by processes that reduce bioavailability (e.g.…”

Section: Introductionmentioning

confidence: 99%

Comparison of naphthalene bioavailability determined by whole-cell biosensing and availability determined by extraction with Tenax

Kohlmeier

Mancuso

Deepthike

et al. 2008

Environmental Pollution

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Genetics of Polycyclic Aromatic Hydrocarbon Metabolism in Diverse Aerobic Bacteria

Cited by 386 publications

References 135 publications

High aromatic ring-cleavage diversity in birch rhizosphere: PAH treatment-specific changes of I.E.3 group extradiol dioxygenases and 16S rRNA bacterial communities in soil

High aromatic ring-cleavage diversity in birch rhizosphere: PAH treatment-specific changes of I.E.3 group extradiol dioxygenases and 16S rRNA bacterial communities in soil

A novel degradation pathway in the assimilation of phenanthrene by Staphylococcus sp. strain PN/Y via meta-cleavage of 2-hydroxy-1-naphthoic acid: formation of trans-2,3-dioxo-5-(2′-hydroxyphenyl)-pent-4-enoic acid

Comparison of naphthalene bioavailability determined by whole-cell biosensing and availability determined by extraction with Tenax

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