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Title: The phn Island: A New Genomic Island Encoding Catabolism of Polynuclear Aromatic Hydrocarbons

Journal Article · · Frontiers in Microbiology

Bacteria are key in the biodegradation of polycyclic aromatic hydrocarbons (PAH), which are widespread environmental pollutants. At least six genotypes of PAH degraders are distinguishable via phylogenies of the ring-hydroxylating dioxygenase (RHD) that initiates bacterial PAH metabolism. A given RHD genotype can be possessed by a variety of bacterial genera, suggesting horizontal gene transfer (HGT) is an important process for dissemination of PAH-degrading genes. But, mechanisms of HGT for most RHD genotypes are unknown. Here, we report in silico and functional analyses of the phenanthrene-degrading bacterium Delftia sp. Cs1-4, a representative of the phnAFK2 RHD group. The phnAFK2 genotype predominates PAH degrader communities in some soils and sediments, but, until now, their genomic biology has not been explored. In the present study, genes for the entire phenanthrene catabolic pathway were discovered on a novel ca. 232 kb genomic island (GEI), now termed the phn island. This GEI had characteristics of an integrative and conjugative element with a mobilization/stabilization system similar to that of SXT/R391-type GEI. But, it could not be grouped with any known GEI, and was the first member of a new GEI class. The island also carried genes predicted to encode: synthesis of quorum sensing signal molecules, fatty acid/polyhydroxyalkanoate biosynthesis, a type IV secretory system, a PRTRC system, DNA mobilization functions and >50 hypothetical proteins. The 50% G + C content of the phn gene cluster differed significantly from the 66.7% G + C level of the island as a whole and the strain Cs1-4 chromosome, indicating a divergent phylogenetic origin for the phn genes. Collectively, these studies added new insights into the genetic elements affecting the PAH biodegradation capacity of microbial communities specifically, and the potential vehicles of HGT in general.

Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Univ. of Wisconsin–Madison; National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231; MCB0920664; CSP795673
OSTI ID:
1628054
Journal Information:
Frontiers in Microbiology, Vol. 3; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (53)

The role of the fatty acid β-oxidation multienzyme complex from Pseudomonas oleovorans in polyhydroxyalkanoate biosynthesis: molecular characterization of the fadBA operon from P. oleovorans and of the enoyl-CoA hydratase genes phaJ from P. oleovorans and Pseudomonas putida journal August 2002
Molecular characteristics of xenobiotic-degrading sphingomonads journal November 2008
Insights into the genetic diversity of initial dioxygenases from PAH-degrading bacteria journal May 2001
Conjugative transfer of preferential utilization of aromatic compounds from Pseudomonas putida CSV86 journal May 2007
Characterization of a phenanthrene degradation plasmid from Alcaligenes faecalis AFK2 journal January 1990
Complete nucleotide sequence and organization of the naphthalene catabolic plasmid pND6-1 from Pseudomonas sp. strain ND6 journal July 2004
Complete Sequence and Genetic Organization of pDTG1, the 83 Kilobase Naphthalene Degradation Plasmid from Pseudomonas putida strain NCIB 9816-4 journal August 2004
Three-dimensional Structure of Iminodisuccinate Epimerase Defines the Fold of the MmgE/PrpD Protein Family journal September 2006
Molecular characterization and properties of (R)-specific enoyl-CoA hydratases from Pseudomonas aeruginosa: metabolic tools for synthesis of polyhydroxyalkanoates via fatty acid ß-oxidation journal January 2003
F factor conjugation is a true type IV secretion system journal July 2003
Genomic islands and the evolution of catabolic pathways in bacteria journal June 2003
Perspectives of medium chain length poly(hydroxyalkanoates), a versatile set of bacterial bioplastics journal June 1999
The mar regulon: multiple resistance to antibiotics and other toxic chemicals journal October 1999
Peer Reviewed: Analytical Applications of Single-Molecule Detection journal June 2002
A Statistical Model for Identifying Proteins by Tandem Mass Spectrometry journal September 2003
Equivalent-Circuit Model for the Thickness-Shear Mode Resonator with a Viscoelastic Film Near Film Resonance journal December 1999
Facilitated Transport of 2,2′,5,5′-Polychlorinated Biphenyl and Phenanthrene by Fullerene Nanoparticles through Sandy Soil Columns journal January 2011
SOS response promotes horizontal dissemination of antibiotic resistance genes journal December 2003
Genomic islands in pathogenic and environmental microorganisms journal May 2004
Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Minireview journal February 2001
The Cyanobacterial Homologue of HCF136/YCF48 Is a Component of an Early Photosystem II Assembly Complex and Is Important for Both the Efficient Assembly and Repair of Photosystem II in Synechocystis sp. PCC 6803 journal June 2008
A putative mobile genetic element carrying a novel type IIF restriction-modification system (PluTI) journal January 2010
ICEberg: a web-based resource for integrative and conjugative elements found in Bacteria journal October 2011
The genome of Polaromonas naphthalenivorans strain CJ2, isolated from coal tar-contaminated sediment, reveals physiological and metabolic versatility and evolution through extensive horizontal gene transfer journal September 2009
Conjugal transfer and mobilization capacity of the completely sequenced naphthalene plasmid pNAH20 from multiplasmid strainPseudomonas fluorescensPC20 journal December 2009
Genomic islands: tools of bacterial horizontal gene transfer and evolution journal March 2009
Combinatorial events of insertion sequences and ICE in Gram-negative bacteria journal September 2011
Soil Type-Dependent Responses to Phenanthrene as Revealed by Determining the Diversity and Abundance of Polycyclic Aromatic Hydrocarbon Ring-Hydroxylating Dioxygenase Genes by Using a Novel PCR Detection System journal July 2010
Characterization of a Polycyclic Aromatic Hydrocarbon Degradation Gene Cluster in a Phenanthrene-Degrading Acidovorax Strain journal May 2009
Phenanthrene-degrading phenotype of Alcaligenes faecalis AFK2 journal February 1982
Degradation of mono-, di-, and trihalogenated benzoic acids by Pseudomonas aeruginosa JB2 journal December 1990
The Biphenyl- and 4-Chlorobiphenyl-Catabolic Transposon Tn 4371 , a Member of a New Family of Genomic Islands Related to IncP and Ti Plasmids journal August 2003
Identification and Functional Analysis of Two Aromatic-Ring-Hydroxylating Dioxygenases from a Sphingomonas Strain That Degrades Various Polycyclic Aromatic Hydrocarbons journal November 2004
Isolation of Soil Bacteria Adapted To Degrade Humic Acid-Sorbed Phenanthrene journal July 2005
The Naphthalene Catabolic ( nag ) Genes of Polaromonas naphthalenivorans CJ2: Evolutionary Implications for Two Gene Clusters and Novel Regulatory Control journal February 2006
The Burkholderia cepacia Epidemic Strain Marker Is Part of a Novel Genomic Island Encoding Both Virulence and Metabolism-Associated Genes in Burkholderia cenocepacia journal March 2004
Predicting Plasmid Promiscuity Based on Genomic Signature journal November 2010
Self-Transmissibility of the Integrative and Conjugative Element ICE Pm1 between Clinical Isolates Requires a Functional Integrase, Relaxase, and Type IV Secretion System journal August 2011
Complete Genome Sequence of the Polycyclic Aromatic Hydrocarbon-Degrading Bacterium Alteromonas sp. Strain SN2 journal August 2011
FabG, an NADPH-Dependent 3-Ketoacyl Reductase of Pseudomonas aeruginosa, Provides Precursors for Medium-Chain-Length Poly-3-Hydroxyalkanoate Biosynthesis in Escherichia coli journal May 2000
A 90-Kilobase Conjugative Chromosomal Element Coding for Biphenyl and Salicylate Catabolism in Pseudomonas putida KF715 journal April 2000
Genomic and Functional Analyses of SXT, an Integrating Antibiotic Resistance Gene Transfer Element Derived from Vibrio cholerae journal August 2002
Control of SXT Integration and Excision journal September 2003
Identification and Characterization of a New Enoyl Coenzyme A Hydratase Involved in Biosynthesis of Medium-Chain-Length Polyhydroxyalkanoates in Recombinant Escherichia coli journal September 2003
Analysis of the sequence and gene products of the transfer region of the F sex factor. journal January 1994
Degradation of phenanthrene and naphthalene by a Burkholderia species strain journal February 2003
Regulation of gene Expression by Reactive Oxygen journal April 1999
Oxygen Activation and Oxygen Toxicity journal June 1982
A new classification system for bacterial Rieske non-heme iron aromatic ring-hydroxylating oxygenases journal January 2008
Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation journal January 2009
Novel aromatic ring-hydroxylating dioxygenase genes from coastal marine sediments of Patagonia journal March 2008
Across Bacterial Phyla, Distantly-Related Genomes with Similar Genomic GC Content Have Similar Patterns of Amino Acid Usage journal March 2011
Development of Tools for Genetic Analysis of Phenanthrene Degradation and Nanopod Production by Delftia sp. Cs1-4 journal January 2011

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