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Comparative Genomic Analysis of Stenotrophomonas maltophilia Strain W18 Reveals Its Adaptative Genomic Features for Degrading Polycyclic Aromatic Hydrocarbons

Polycyclic aromatic hydrocarbons (PAHs) are hazardous pollutants that are ubiquitous in the environment. Numerous bacteria have evolved to have degrading genes or pathways to degrade PAHs. Stenotrophomonas maltophilia strain W18 was found to be able to degrade PAHs. Including 43 other complete genom...

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Autores principales: Xiao, Yaqian, Jiang, Ruhan, Wu, Xiaoxiong, Zhong, Qi, Li, Yi, Wang, Hongqi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8612148/
https://www.ncbi.nlm.nih.gov/pubmed/34817285
http://dx.doi.org/10.1128/Spectrum.01420-21
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author Xiao, Yaqian
Jiang, Ruhan
Wu, Xiaoxiong
Zhong, Qi
Li, Yi
Wang, Hongqi
author_facet Xiao, Yaqian
Jiang, Ruhan
Wu, Xiaoxiong
Zhong, Qi
Li, Yi
Wang, Hongqi
author_sort Xiao, Yaqian
collection PubMed
description Polycyclic aromatic hydrocarbons (PAHs) are hazardous pollutants that are ubiquitous in the environment. Numerous bacteria have evolved to have degrading genes or pathways to degrade PAHs. Stenotrophomonas maltophilia strain W18 was found to be able to degrade PAHs. Including 43 other complete genome sequences of S. maltophilia strains, we performed a comparative genomic analysis of 44 S. maltophilia strains by running OrthoFinder. A KEGG pathway enrichment analysis of environmental and clinical isolates of S. maltophilia revealed that environmental isolates tended to enhance gene functions such as “energy metabolism,” “amino acid metabolism,” “xenobiotic biodegradation and metabolism,” and “folding, sorting, and degradation.” The pangenome of the 44 S. maltophilia strains was open, while the core genome was estimated to reach a steady plateau. Based on gene annotations, we inferred that most of the degradation potential came from the core genome of S. maltophilia, while character genes and accessory genes also contributed to the degradation ability of S. maltophilia W18. The genes expression level of core genes, character genes and accessory genes were proved by RT-qPCR experiment, and accessory genes encoding alcohol dehydrogenase were upregulated most compared with genes with similar functions. We performed a credible comparative genomic analysis of S. maltophilia strains. S. maltophilia W18 was set as a model PAH-degrading bacterium of this species in this study, which would provide guidance for understanding and predicting the degradation mechanisms of other PAH-degrading S. maltophilia strains lacking complete genome data or waiting to be determined. IMPORTANCE This study provided the latest comparative genomic analysis on Stenotrophomonas maltophilia strains and focused on analyzing their genomic features that allow them to adapt to natural environments. In this study, we set S. maltophilia W18 as a typical PAH-degrading strain of this species. By discussing the genomic adaptative features of degrading PAH, we can predict genomic adaptative features of other S. maltophilia PAH-degrading strains since the core function of this species is stable. The gene functions of how S. maltophilia environmental isolates are enhanced for adaptation to various natural environments compared with clinical isolates have been revealed. Combined with a pangenome analysis and RT-qPCR results, we have proved that core genes, character genes, and accessory genes are all involved in PAH degradation. Accessory genes encoding alcohol dehydrogenase were upregulated most compared with core and character genes with similar functions, which suggests that PAH metabolization potential might be enhanced by horizontal gene transfer.
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spelling pubmed-86121482021-11-29 Comparative Genomic Analysis of Stenotrophomonas maltophilia Strain W18 Reveals Its Adaptative Genomic Features for Degrading Polycyclic Aromatic Hydrocarbons Xiao, Yaqian Jiang, Ruhan Wu, Xiaoxiong Zhong, Qi Li, Yi Wang, Hongqi Microbiol Spectr Research Article Polycyclic aromatic hydrocarbons (PAHs) are hazardous pollutants that are ubiquitous in the environment. Numerous bacteria have evolved to have degrading genes or pathways to degrade PAHs. Stenotrophomonas maltophilia strain W18 was found to be able to degrade PAHs. Including 43 other complete genome sequences of S. maltophilia strains, we performed a comparative genomic analysis of 44 S. maltophilia strains by running OrthoFinder. A KEGG pathway enrichment analysis of environmental and clinical isolates of S. maltophilia revealed that environmental isolates tended to enhance gene functions such as “energy metabolism,” “amino acid metabolism,” “xenobiotic biodegradation and metabolism,” and “folding, sorting, and degradation.” The pangenome of the 44 S. maltophilia strains was open, while the core genome was estimated to reach a steady plateau. Based on gene annotations, we inferred that most of the degradation potential came from the core genome of S. maltophilia, while character genes and accessory genes also contributed to the degradation ability of S. maltophilia W18. The genes expression level of core genes, character genes and accessory genes were proved by RT-qPCR experiment, and accessory genes encoding alcohol dehydrogenase were upregulated most compared with genes with similar functions. We performed a credible comparative genomic analysis of S. maltophilia strains. S. maltophilia W18 was set as a model PAH-degrading bacterium of this species in this study, which would provide guidance for understanding and predicting the degradation mechanisms of other PAH-degrading S. maltophilia strains lacking complete genome data or waiting to be determined. IMPORTANCE This study provided the latest comparative genomic analysis on Stenotrophomonas maltophilia strains and focused on analyzing their genomic features that allow them to adapt to natural environments. In this study, we set S. maltophilia W18 as a typical PAH-degrading strain of this species. By discussing the genomic adaptative features of degrading PAH, we can predict genomic adaptative features of other S. maltophilia PAH-degrading strains since the core function of this species is stable. The gene functions of how S. maltophilia environmental isolates are enhanced for adaptation to various natural environments compared with clinical isolates have been revealed. Combined with a pangenome analysis and RT-qPCR results, we have proved that core genes, character genes, and accessory genes are all involved in PAH degradation. Accessory genes encoding alcohol dehydrogenase were upregulated most compared with core and character genes with similar functions, which suggests that PAH metabolization potential might be enhanced by horizontal gene transfer. American Society for Microbiology 2021-11-24 /pmc/articles/PMC8612148/ /pubmed/34817285 http://dx.doi.org/10.1128/Spectrum.01420-21 Text en Copyright © 2021 Xiao et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Xiao, Yaqian
Jiang, Ruhan
Wu, Xiaoxiong
Zhong, Qi
Li, Yi
Wang, Hongqi
Comparative Genomic Analysis of Stenotrophomonas maltophilia Strain W18 Reveals Its Adaptative Genomic Features for Degrading Polycyclic Aromatic Hydrocarbons
title Comparative Genomic Analysis of Stenotrophomonas maltophilia Strain W18 Reveals Its Adaptative Genomic Features for Degrading Polycyclic Aromatic Hydrocarbons
title_full Comparative Genomic Analysis of Stenotrophomonas maltophilia Strain W18 Reveals Its Adaptative Genomic Features for Degrading Polycyclic Aromatic Hydrocarbons
title_fullStr Comparative Genomic Analysis of Stenotrophomonas maltophilia Strain W18 Reveals Its Adaptative Genomic Features for Degrading Polycyclic Aromatic Hydrocarbons
title_full_unstemmed Comparative Genomic Analysis of Stenotrophomonas maltophilia Strain W18 Reveals Its Adaptative Genomic Features for Degrading Polycyclic Aromatic Hydrocarbons
title_short Comparative Genomic Analysis of Stenotrophomonas maltophilia Strain W18 Reveals Its Adaptative Genomic Features for Degrading Polycyclic Aromatic Hydrocarbons
title_sort comparative genomic analysis of stenotrophomonas maltophilia strain w18 reveals its adaptative genomic features for degrading polycyclic aromatic hydrocarbons
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8612148/
https://www.ncbi.nlm.nih.gov/pubmed/34817285
http://dx.doi.org/10.1128/Spectrum.01420-21
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