New Plant Growth-Promoting, Chromium-Detoxifying Microbacterium Species Isolated From a Tannery Wastewater: Performance and Genomic Insights

Hexavalent chromium [Cr(VI)], widely generated by tannery activities, is considered among the most toxic substances and causes a serious damage for the environment and for human health. Interestingly, some microorganisms have a potential of bioremediation of chromium-contaminated wastewaters and soi...

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Main Authors: Rania Ouertani, Awatef Ouertani, Mouna Mahjoubi, Yosra Bousselmi, Afef Najjari, Hanene Cherif, Asma Chamkhi, Amor Mosbah, Hechmi Khdhira, Haitham Sghaier, Habib Chouchane, Ameur Cherif, Mohamed Neifar
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Bioengineering and Biotechnology
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Online Access:https://www.frontiersin.org/article/10.3389/fbioe.2020.00521/full
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author Rania Ouertani
Rania Ouertani
Awatef Ouertani
Mouna Mahjoubi
Yosra Bousselmi
Afef Najjari
Hanene Cherif
Asma Chamkhi
Amor Mosbah
Hechmi Khdhira
Haitham Sghaier
Haitham Sghaier
Habib Chouchane
Ameur Cherif
Mohamed Neifar
spellingShingle Rania Ouertani
Rania Ouertani
Awatef Ouertani
Mouna Mahjoubi
Yosra Bousselmi
Afef Najjari
Hanene Cherif
Asma Chamkhi
Amor Mosbah
Hechmi Khdhira
Haitham Sghaier
Haitham Sghaier
Habib Chouchane
Ameur Cherif
Mohamed Neifar
New Plant Growth-Promoting, Chromium-Detoxifying Microbacterium Species Isolated From a Tannery Wastewater: Performance and Genomic Insights
Frontiers in Bioengineering and Biotechnology
actinobacterium
bioremediation
genome annotation
heavy metals
plant growth promotion
tannery wastewater
author_facet Rania Ouertani
Rania Ouertani
Awatef Ouertani
Mouna Mahjoubi
Yosra Bousselmi
Afef Najjari
Hanene Cherif
Asma Chamkhi
Amor Mosbah
Hechmi Khdhira
Haitham Sghaier
Haitham Sghaier
Habib Chouchane
Ameur Cherif
Mohamed Neifar
author_sort Rania Ouertani
title New Plant Growth-Promoting, Chromium-Detoxifying Microbacterium Species Isolated From a Tannery Wastewater: Performance and Genomic Insights
title_short New Plant Growth-Promoting, Chromium-Detoxifying Microbacterium Species Isolated From a Tannery Wastewater: Performance and Genomic Insights
title_full New Plant Growth-Promoting, Chromium-Detoxifying Microbacterium Species Isolated From a Tannery Wastewater: Performance and Genomic Insights
title_fullStr New Plant Growth-Promoting, Chromium-Detoxifying Microbacterium Species Isolated From a Tannery Wastewater: Performance and Genomic Insights
title_full_unstemmed New Plant Growth-Promoting, Chromium-Detoxifying Microbacterium Species Isolated From a Tannery Wastewater: Performance and Genomic Insights
title_sort new plant growth-promoting, chromium-detoxifying microbacterium species isolated from a tannery wastewater: performance and genomic insights
publisher Frontiers Media S.A.
series Frontiers in Bioengineering and Biotechnology
issn 2296-4185
publishDate 2020-07-01
description Hexavalent chromium [Cr(VI)], widely generated by tannery activities, is considered among the most toxic substances and causes a serious damage for the environment and for human health. Interestingly, some microorganisms have a potential of bioremediation of chromium-contaminated wastewaters and soils through the reduction of Cr(VI) (soluble and harmful form) into Cr(III) (stable and non-toxic form). Here, we present the full genome sequence of a novel heavy-metal-resistant, plant growth-promoting bacterium (PGPB), Microbacterium metallidurans TL13, which was isolated from a Tunisian leather industry. The strain TL13 was resistant to many heavy metals, such as chromium, copper, nickel, cobalt, and arsenic. The 50% TL13 growth inhibitory concentration (IC50) values of HgCl2, CoCl2, K2Cr2O7, CuSO4, NiCl2, FeSO4, and Na2HAsO4 are 368, 445, 676, 1,590, 1,680, 4,403, and 7,007 mg/L, respectively, with the following toxicity order: HgCl2 > CoCl2 > K2Cr2O7 > CuSO4 > NiCl2 > FeSO4 > Na2HAsO4. This new strain was also able to promote the growth of the hybrid tomato (Elika F1) under chromium metal stress. Its whole genome sequence length was estimated to be 3,587,460 bp (3,393 coding sequences) with a G + C content of 70.7%. Functional annotation of the genome of TL13 revealed the presence of open reading frames (ORFs) involved in adaptation to metal stress, such as the chromate transport protein, cobalt–zinc–cadmium resistance protein, copper resistance protein, copper responsive transcriptional regulator, multidrug resistance transporters, arsenical resistance operon repressor, arsenate reductase, arsenic resistance protein, mercuric resistance operon regulatory protein, mercuric ion reductase, and organomercurial lyase. Moreover, genes for the production of glutathione peroxidase, catalase, superoxide dismutase, and thioredoxin reductase, which confer a higher tolerance to oxidative/metal stresses, were identified in TL13 genome. In addition, genes for heat shock tolerance, cold shock tolerance, glycine-betaine production, mineral phosphate solubilization, ammonia assimilation, siderophores, exopolysaccharides, polyketides, and lytic enzymes (cellulase, chitinase, and proteases) production that enable bacteria to survive biotic/abiotic stress and to promote plant growth and health were also revealed. Based on genome analysis and experimental approaches, strain TL13 appears to have evolved from various metabolic strategies and could play a role in ensuring sustainable environmental and agricultural systems.
topic actinobacterium
bioremediation
genome annotation
heavy metals
plant growth promotion
tannery wastewater
url https://www.frontiersin.org/article/10.3389/fbioe.2020.00521/full
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spelling doaj-7754cddde79940b589693a104678ae582020-11-25T03:51:59ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852020-07-01810.3389/fbioe.2020.00521523323New Plant Growth-Promoting, Chromium-Detoxifying Microbacterium Species Isolated From a Tannery Wastewater: Performance and Genomic InsightsRania Ouertani0Rania Ouertani1Awatef Ouertani2Mouna Mahjoubi3Yosra Bousselmi4Afef Najjari5Hanene Cherif6Asma Chamkhi7Amor Mosbah8Hechmi Khdhira9Haitham Sghaier10Haitham Sghaier11Habib Chouchane12Ameur Cherif13Mohamed Neifar14Univ. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaLaboratory of Microorganisms and Active Biomolecules, MBA-LR03ES03, Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaLaboratory of Microorganisms and Active Biomolecules, MBA-LR03ES03, Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaManagement Environment Responsible in Tanneries Mégisseries du Maghreb, TMM, Grombalia, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaLaboratory “Energy and Matter for Development of Nuclear Sciences” (LR16CNSTN02), National Center for Nuclear Sciences and Technology (CNSTN), Sidi Thabet Technopark, Sidi Thabet, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaUniv. Manouba, ISBST, BVBGR-LR11ES31, Biotechpole Sidi Thabet, Sidi Thabet, TunisiaHexavalent chromium [Cr(VI)], widely generated by tannery activities, is considered among the most toxic substances and causes a serious damage for the environment and for human health. Interestingly, some microorganisms have a potential of bioremediation of chromium-contaminated wastewaters and soils through the reduction of Cr(VI) (soluble and harmful form) into Cr(III) (stable and non-toxic form). Here, we present the full genome sequence of a novel heavy-metal-resistant, plant growth-promoting bacterium (PGPB), Microbacterium metallidurans TL13, which was isolated from a Tunisian leather industry. The strain TL13 was resistant to many heavy metals, such as chromium, copper, nickel, cobalt, and arsenic. The 50% TL13 growth inhibitory concentration (IC50) values of HgCl2, CoCl2, K2Cr2O7, CuSO4, NiCl2, FeSO4, and Na2HAsO4 are 368, 445, 676, 1,590, 1,680, 4,403, and 7,007 mg/L, respectively, with the following toxicity order: HgCl2 > CoCl2 > K2Cr2O7 > CuSO4 > NiCl2 > FeSO4 > Na2HAsO4. This new strain was also able to promote the growth of the hybrid tomato (Elika F1) under chromium metal stress. Its whole genome sequence length was estimated to be 3,587,460 bp (3,393 coding sequences) with a G + C content of 70.7%. Functional annotation of the genome of TL13 revealed the presence of open reading frames (ORFs) involved in adaptation to metal stress, such as the chromate transport protein, cobalt–zinc–cadmium resistance protein, copper resistance protein, copper responsive transcriptional regulator, multidrug resistance transporters, arsenical resistance operon repressor, arsenate reductase, arsenic resistance protein, mercuric resistance operon regulatory protein, mercuric ion reductase, and organomercurial lyase. Moreover, genes for the production of glutathione peroxidase, catalase, superoxide dismutase, and thioredoxin reductase, which confer a higher tolerance to oxidative/metal stresses, were identified in TL13 genome. In addition, genes for heat shock tolerance, cold shock tolerance, glycine-betaine production, mineral phosphate solubilization, ammonia assimilation, siderophores, exopolysaccharides, polyketides, and lytic enzymes (cellulase, chitinase, and proteases) production that enable bacteria to survive biotic/abiotic stress and to promote plant growth and health were also revealed. Based on genome analysis and experimental approaches, strain TL13 appears to have evolved from various metabolic strategies and could play a role in ensuring sustainable environmental and agricultural systems.https://www.frontiersin.org/article/10.3389/fbioe.2020.00521/fullactinobacteriumbioremediationgenome annotationheavy metalsplant growth promotiontannery wastewater