Cargando…

Genome Sequence of the Deltaproteobacterial Strain NaphS2 and Analysis of Differential Gene Expression during Anaerobic Growth on Naphthalene

BACKGROUND: Anaerobic polycyclic hydrocarbon (PAH) degradation coupled to sulfate reduction may be an important mechanism for in situ remediation of contaminated sediments. Steps involved in the anaerobic degradation of 2-methylnaphthalene have been described in the sulfate reducing strains NaphS3,...

Descripción completa

Detalles Bibliográficos
Autores principales: DiDonato, Raymond J., Young, Nelson D., Butler, Jessica E., Chin, Kuk-Jeong, Hixson, Kim K., Mouser, Paula, Lipton, Mary S., DeBoy, Robert, Methé, Barbara A.
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2988823/
https://www.ncbi.nlm.nih.gov/pubmed/21124915
http://dx.doi.org/10.1371/journal.pone.0014072
_version_ 1782192289838268416
author DiDonato, Raymond J.
Young, Nelson D.
Butler, Jessica E.
Chin, Kuk-Jeong
Hixson, Kim K.
Mouser, Paula
Lipton, Mary S.
DeBoy, Robert
Methé, Barbara A.
author_facet DiDonato, Raymond J.
Young, Nelson D.
Butler, Jessica E.
Chin, Kuk-Jeong
Hixson, Kim K.
Mouser, Paula
Lipton, Mary S.
DeBoy, Robert
Methé, Barbara A.
author_sort DiDonato, Raymond J.
collection PubMed
description BACKGROUND: Anaerobic polycyclic hydrocarbon (PAH) degradation coupled to sulfate reduction may be an important mechanism for in situ remediation of contaminated sediments. Steps involved in the anaerobic degradation of 2-methylnaphthalene have been described in the sulfate reducing strains NaphS3, NaphS6 and N47. Evidence from N47 suggests that naphthalene degradation involves 2-methylnaphthalene as an intermediate, whereas evidence in NaphS2, NaphS3 and NaphS6 suggests a mechanism for naphthalene degradation that does not involve 2-methylnaphthalene. To further characterize pathways involved in naphthalene degradation in NaphS2, the draft genome was sequenced, and gene and protein expression examined. RESULTS: Draft genome sequencing, gene expression analysis, and proteomic analysis revealed that NaphS2 degrades naphthoyl-CoA in a manner analogous to benzoyl-CoA degradation. Genes including the previously characterized NmsA, thought to encode an enzyme necessary for 2-methylnaphthalene metabolism, were not upregulated during growth of NaphS2 on naphthalene, nor were the corresponding protein products. NaphS2 may possess a non-classical dearomatizing enzyme for benzoate degradation, similar to one previously characterized in Geobacter metallireducens. Identification of genes involved in toluene degradation in NaphS2 led us to determine that NaphS2 degrades toluene, a previously unreported capacity. The genome sequence also suggests that NaphS2 may degrade other monoaromatic compounds. CONCLUSION: This study demonstrates that steps leading to the degradation of 2-naphthoyl-CoA are conserved between NaphS2 and N47, however while NaphS2 possesses the capacity to degrade 2-methylnaphthalene, naphthalene degradation likely does not proceed via 2-methylnaphthalene. Instead, carboxylation or another form of activation may serve as the first step in naphthalene degradation. Degradation of toluene and 2-methylnaphthalene, and the presence of at least one bss-like and bbs-like gene cluster in this organism, suggests that NaphS2 degrades both compounds via parallel mechanisms. Elucidation of the key genes necessary for anaerobic naphthalene degradation may provide the ability to track naphthalene degradation through in situ transcript monitoring.
format Text
id pubmed-2988823
institution National Center for Biotechnology Information
language English
publishDate 2010
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-29888232010-12-01 Genome Sequence of the Deltaproteobacterial Strain NaphS2 and Analysis of Differential Gene Expression during Anaerobic Growth on Naphthalene DiDonato, Raymond J. Young, Nelson D. Butler, Jessica E. Chin, Kuk-Jeong Hixson, Kim K. Mouser, Paula Lipton, Mary S. DeBoy, Robert Methé, Barbara A. PLoS One Research Article BACKGROUND: Anaerobic polycyclic hydrocarbon (PAH) degradation coupled to sulfate reduction may be an important mechanism for in situ remediation of contaminated sediments. Steps involved in the anaerobic degradation of 2-methylnaphthalene have been described in the sulfate reducing strains NaphS3, NaphS6 and N47. Evidence from N47 suggests that naphthalene degradation involves 2-methylnaphthalene as an intermediate, whereas evidence in NaphS2, NaphS3 and NaphS6 suggests a mechanism for naphthalene degradation that does not involve 2-methylnaphthalene. To further characterize pathways involved in naphthalene degradation in NaphS2, the draft genome was sequenced, and gene and protein expression examined. RESULTS: Draft genome sequencing, gene expression analysis, and proteomic analysis revealed that NaphS2 degrades naphthoyl-CoA in a manner analogous to benzoyl-CoA degradation. Genes including the previously characterized NmsA, thought to encode an enzyme necessary for 2-methylnaphthalene metabolism, were not upregulated during growth of NaphS2 on naphthalene, nor were the corresponding protein products. NaphS2 may possess a non-classical dearomatizing enzyme for benzoate degradation, similar to one previously characterized in Geobacter metallireducens. Identification of genes involved in toluene degradation in NaphS2 led us to determine that NaphS2 degrades toluene, a previously unreported capacity. The genome sequence also suggests that NaphS2 may degrade other monoaromatic compounds. CONCLUSION: This study demonstrates that steps leading to the degradation of 2-naphthoyl-CoA are conserved between NaphS2 and N47, however while NaphS2 possesses the capacity to degrade 2-methylnaphthalene, naphthalene degradation likely does not proceed via 2-methylnaphthalene. Instead, carboxylation or another form of activation may serve as the first step in naphthalene degradation. Degradation of toluene and 2-methylnaphthalene, and the presence of at least one bss-like and bbs-like gene cluster in this organism, suggests that NaphS2 degrades both compounds via parallel mechanisms. Elucidation of the key genes necessary for anaerobic naphthalene degradation may provide the ability to track naphthalene degradation through in situ transcript monitoring. Public Library of Science 2010-11-19 /pmc/articles/PMC2988823/ /pubmed/21124915 http://dx.doi.org/10.1371/journal.pone.0014072 Text en DiDonato Jr. et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
DiDonato, Raymond J.
Young, Nelson D.
Butler, Jessica E.
Chin, Kuk-Jeong
Hixson, Kim K.
Mouser, Paula
Lipton, Mary S.
DeBoy, Robert
Methé, Barbara A.
Genome Sequence of the Deltaproteobacterial Strain NaphS2 and Analysis of Differential Gene Expression during Anaerobic Growth on Naphthalene
title Genome Sequence of the Deltaproteobacterial Strain NaphS2 and Analysis of Differential Gene Expression during Anaerobic Growth on Naphthalene
title_full Genome Sequence of the Deltaproteobacterial Strain NaphS2 and Analysis of Differential Gene Expression during Anaerobic Growth on Naphthalene
title_fullStr Genome Sequence of the Deltaproteobacterial Strain NaphS2 and Analysis of Differential Gene Expression during Anaerobic Growth on Naphthalene
title_full_unstemmed Genome Sequence of the Deltaproteobacterial Strain NaphS2 and Analysis of Differential Gene Expression during Anaerobic Growth on Naphthalene
title_short Genome Sequence of the Deltaproteobacterial Strain NaphS2 and Analysis of Differential Gene Expression during Anaerobic Growth on Naphthalene
title_sort genome sequence of the deltaproteobacterial strain naphs2 and analysis of differential gene expression during anaerobic growth on naphthalene
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2988823/
https://www.ncbi.nlm.nih.gov/pubmed/21124915
http://dx.doi.org/10.1371/journal.pone.0014072
work_keys_str_mv AT didonatoraymondj genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene
AT youngnelsond genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene
AT butlerjessicae genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene
AT chinkukjeong genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene
AT hixsonkimk genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene
AT mouserpaula genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene
AT liptonmarys genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene
AT deboyrobert genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene
AT methebarbaraa genomesequenceofthedeltaproteobacterialstrainnaphs2andanalysisofdifferentialgeneexpressionduringanaerobicgrowthonnaphthalene