Isolation of Pseudomonas aromaticivorans sp. nov from a hydrocarbon-contaminated groundwater capable of degrading benzene-, toluene-, m- and p-xylene under microaerobic conditions

Members of the genus Pseudomonas are known to be widespread in hydrocarbon contaminated environments because of their remarkable ability to degrade a variety of petroleum hydrocarbons, including BTEX (benzene, toluene, ethylbenzene and xylene) compounds. During an enrichment investigation which aime...

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Main Authors: Sinchan Banerjee, Anna Bedics, Erika Tóth, Balázs Kriszt, André R. Soares, Károly Bóka, András Táncsics
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.929128/full
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author Sinchan Banerjee
Anna Bedics
Erika Tóth
Balázs Kriszt
André R. Soares
Károly Bóka
András Táncsics
author_facet Sinchan Banerjee
Anna Bedics
Erika Tóth
Balázs Kriszt
André R. Soares
Károly Bóka
András Táncsics
author_sort Sinchan Banerjee
collection DOAJ
description Members of the genus Pseudomonas are known to be widespread in hydrocarbon contaminated environments because of their remarkable ability to degrade a variety of petroleum hydrocarbons, including BTEX (benzene, toluene, ethylbenzene and xylene) compounds. During an enrichment investigation which aimed to study microaerobic xylene degradation in a legacy petroleum hydrocarbon-contaminated groundwater, a novel Gram-stain-negative, aerobic, motile and rod-shaped bacterial strain, designated as MAP12T was isolated. It was capable of degrading benzene, toluene, meta- and para- xylene effectively under both aerobic and microaerobic conditions. The 16S rRNA gene sequence analysis revealed that strain MAP12T belongs to the genus Pseudomonas, with the highest 16S rRNA gene similarity to Pseudomonas linyingensis LYBRD3-7T (98.42%), followed by Pseudomonas sagittaria JCM 18195T (98.29%) and Pseudomonas alcaliphila JCM 10630T (98.08%). Phylogenomic tree constructed using a concatenated alignment of 92 core genes indicated that strain MAP12T is distinct from any known Pseudomonas species. The draft genome sequence of strain MAP12T is 4.36 Mb long, and the G+C content of MAP12T genome is 65.8%. Orthologous average nucleotide identity (OrthoANI) and digital DNA–DNA hybridization (dDDH) analyses confirmed that strain MAP12T is distinctly separated from its closest neighbors (OrthoANI < 89 %; dDDH < 36%). Though several members of the genus Pseudomonas are well known for their aerobic BTEX degradation capability, this is the first report of a novel Pseudomonas species capable of degrading xylene under microaerobic conditions. By applying genome-resolved metagenomics, we were able to partially reconstruct the genome of strain MAP12T from metagenomics sequence data and showed that strain MAP12T was an abundant member of the xylene-degrading bacterial community under microaerobic conditions. Strain MAP12T contains ubiquinone 9 (Q9) as the major respiratory quinone and diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine as major polar lipids. The major cellular fatty acids of strain MAP12T are summed feature 3 (C16:1ω6c and/or C16:1ω7c), C16:0 and summed feature 8 (C18:1ω6c and/or C18:1ω7c). The results of this polyphasic study support that strain MAP12T represents a novel species of the genus Pseudomonas, hence the name of Pseudomonas aromaticivorans sp. nov. is proposed for this strain considering its aromatic hydrocarbon degradation capability. The type strain is MAP12T (=LMG 32466, =NCAIM B.02668).
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spelling doaj.art-cfc1cdb35bc6453f9f5b92009f890ea42022-12-22T04:30:25ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-09-011310.3389/fmicb.2022.929128929128Isolation of Pseudomonas aromaticivorans sp. nov from a hydrocarbon-contaminated groundwater capable of degrading benzene-, toluene-, m- and p-xylene under microaerobic conditionsSinchan Banerjee0Anna Bedics1Erika Tóth2Balázs Kriszt3André R. Soares4Károly Bóka5András Táncsics6Department of Molecular Ecology, Institute of Aquaculture and Environmental Safety, Hungarian University of Agriculture and Life Sciences, Gödöllő, HungaryDepartment of Molecular Ecology, Institute of Aquaculture and Environmental Safety, Hungarian University of Agriculture and Life Sciences, Gödöllő, HungaryDepartment of Microbiology, Eötvös Loránd University, Budapest, HungaryDepartment of Environmental Safety, Institute of Aquaculture and Environmental Safety, Hungarian University of Agriculture and Life Sciences, Gödöllő, HungaryGroup for Aquatic Microbial Ecology, Institute for Environmental Microbiology and Biotechnology, University of Duisburg-Essen, Essen, GermanyDepartment of Plant Anatomy, Eötvös Loránd University, Budapest, HungaryDepartment of Molecular Ecology, Institute of Aquaculture and Environmental Safety, Hungarian University of Agriculture and Life Sciences, Gödöllő, HungaryMembers of the genus Pseudomonas are known to be widespread in hydrocarbon contaminated environments because of their remarkable ability to degrade a variety of petroleum hydrocarbons, including BTEX (benzene, toluene, ethylbenzene and xylene) compounds. During an enrichment investigation which aimed to study microaerobic xylene degradation in a legacy petroleum hydrocarbon-contaminated groundwater, a novel Gram-stain-negative, aerobic, motile and rod-shaped bacterial strain, designated as MAP12T was isolated. It was capable of degrading benzene, toluene, meta- and para- xylene effectively under both aerobic and microaerobic conditions. The 16S rRNA gene sequence analysis revealed that strain MAP12T belongs to the genus Pseudomonas, with the highest 16S rRNA gene similarity to Pseudomonas linyingensis LYBRD3-7T (98.42%), followed by Pseudomonas sagittaria JCM 18195T (98.29%) and Pseudomonas alcaliphila JCM 10630T (98.08%). Phylogenomic tree constructed using a concatenated alignment of 92 core genes indicated that strain MAP12T is distinct from any known Pseudomonas species. The draft genome sequence of strain MAP12T is 4.36 Mb long, and the G+C content of MAP12T genome is 65.8%. Orthologous average nucleotide identity (OrthoANI) and digital DNA–DNA hybridization (dDDH) analyses confirmed that strain MAP12T is distinctly separated from its closest neighbors (OrthoANI < 89 %; dDDH < 36%). Though several members of the genus Pseudomonas are well known for their aerobic BTEX degradation capability, this is the first report of a novel Pseudomonas species capable of degrading xylene under microaerobic conditions. By applying genome-resolved metagenomics, we were able to partially reconstruct the genome of strain MAP12T from metagenomics sequence data and showed that strain MAP12T was an abundant member of the xylene-degrading bacterial community under microaerobic conditions. Strain MAP12T contains ubiquinone 9 (Q9) as the major respiratory quinone and diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine as major polar lipids. The major cellular fatty acids of strain MAP12T are summed feature 3 (C16:1ω6c and/or C16:1ω7c), C16:0 and summed feature 8 (C18:1ω6c and/or C18:1ω7c). The results of this polyphasic study support that strain MAP12T represents a novel species of the genus Pseudomonas, hence the name of Pseudomonas aromaticivorans sp. nov. is proposed for this strain considering its aromatic hydrocarbon degradation capability. The type strain is MAP12T (=LMG 32466, =NCAIM B.02668).https://www.frontiersin.org/articles/10.3389/fmicb.2022.929128/fullbiodegradationxyleneBTEXPseudomonagroundwater
spellingShingle Sinchan Banerjee
Anna Bedics
Erika Tóth
Balázs Kriszt
André R. Soares
Károly Bóka
András Táncsics
Isolation of Pseudomonas aromaticivorans sp. nov from a hydrocarbon-contaminated groundwater capable of degrading benzene-, toluene-, m- and p-xylene under microaerobic conditions
Frontiers in Microbiology
biodegradation
xylene
BTEX
Pseudomona
groundwater
title Isolation of Pseudomonas aromaticivorans sp. nov from a hydrocarbon-contaminated groundwater capable of degrading benzene-, toluene-, m- and p-xylene under microaerobic conditions
title_full Isolation of Pseudomonas aromaticivorans sp. nov from a hydrocarbon-contaminated groundwater capable of degrading benzene-, toluene-, m- and p-xylene under microaerobic conditions
title_fullStr Isolation of Pseudomonas aromaticivorans sp. nov from a hydrocarbon-contaminated groundwater capable of degrading benzene-, toluene-, m- and p-xylene under microaerobic conditions
title_full_unstemmed Isolation of Pseudomonas aromaticivorans sp. nov from a hydrocarbon-contaminated groundwater capable of degrading benzene-, toluene-, m- and p-xylene under microaerobic conditions
title_short Isolation of Pseudomonas aromaticivorans sp. nov from a hydrocarbon-contaminated groundwater capable of degrading benzene-, toluene-, m- and p-xylene under microaerobic conditions
title_sort isolation of pseudomonas aromaticivorans sp nov from a hydrocarbon contaminated groundwater capable of degrading benzene toluene m and p xylene under microaerobic conditions
topic biodegradation
xylene
BTEX
Pseudomona
groundwater
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.929128/full
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