Comparative analysis reveals the modular functional structure of conjugative megaplasmid pTTS12 of Pseudomonas putida S12: A paradigm for transferable traits, plasmid stability, and inheritance?

Originating from various environmental niches, large numbers of bacterial plasmids have been found carrying heavy metal and antibiotic resistance genes, degradation pathways and specific transporter genes for organic solvents or aromatic compounds. Such genes may constitute promising candidates for...

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Main Authors: Hadiastri Kusumawardhani, Rohola Hosseini, Jo-Anne Verschoor, Johannes H. de Winde
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.2022.1001472/full
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author Hadiastri Kusumawardhani
Hadiastri Kusumawardhani
Rohola Hosseini
Jo-Anne Verschoor
Johannes H. de Winde
author_facet Hadiastri Kusumawardhani
Hadiastri Kusumawardhani
Rohola Hosseini
Jo-Anne Verschoor
Johannes H. de Winde
author_sort Hadiastri Kusumawardhani
collection DOAJ
description Originating from various environmental niches, large numbers of bacterial plasmids have been found carrying heavy metal and antibiotic resistance genes, degradation pathways and specific transporter genes for organic solvents or aromatic compounds. Such genes may constitute promising candidates for novel synthetic biology applications. Our systematic analysis of gene clusters encoded on megaplasmid pTTS12 from Pseudomonas putida S12 underscores that a large portion of its genes is involved in stress response to increase survival under harsh conditions like the presence of heavy metal and organic solvent. We investigated putative roles of genes encoded on pTTS12 and further elaborated on their roles in the establishment and maintenance under several stress conditions, specifically focusing on solvent tolerance in P. putida strains. The backbone of pTTS12 was found to be closely related to that of the carbapenem-resistance plasmid pOZ176, member of the IncP-2 incompatibility group, although the carbapenem resistance cassette is absent from pTTS12. Megaplasmid pTTS12 contains multiple transposon-flanked cassettes mediating resistance to various heavy metals such as tellurite, chromate (Tn7), and mercury (Tn5053 and Tn5563). Additionally, pTTS12 also contains a P-type, Type IV secretion system (T4SS) supporting self-transfer to other P. putida strains. This study increases our understanding in the modular structure of pTTS12 as a member of IncP-2 plasmid family and several promising exchangeable gene clusters to construct robust microbial hosts for biotechnology applications.
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spelling doaj.art-e79d287d1ff344f5b66a752582c6c8fb2023-03-13T11:56:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-09-011310.3389/fmicb.2022.10014721001472Comparative analysis reveals the modular functional structure of conjugative megaplasmid pTTS12 of Pseudomonas putida S12: A paradigm for transferable traits, plasmid stability, and inheritance?Hadiastri Kusumawardhani0Hadiastri Kusumawardhani1Rohola Hosseini2Jo-Anne Verschoor3Johannes H. de Winde4Institute of Biology Leiden, Leiden University, Leiden, NetherlandsDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, SwitzerlandInstitute of Biology Leiden, Leiden University, Leiden, NetherlandsInstitute of Biology Leiden, Leiden University, Leiden, NetherlandsInstitute of Biology Leiden, Leiden University, Leiden, NetherlandsOriginating from various environmental niches, large numbers of bacterial plasmids have been found carrying heavy metal and antibiotic resistance genes, degradation pathways and specific transporter genes for organic solvents or aromatic compounds. Such genes may constitute promising candidates for novel synthetic biology applications. Our systematic analysis of gene clusters encoded on megaplasmid pTTS12 from Pseudomonas putida S12 underscores that a large portion of its genes is involved in stress response to increase survival under harsh conditions like the presence of heavy metal and organic solvent. We investigated putative roles of genes encoded on pTTS12 and further elaborated on their roles in the establishment and maintenance under several stress conditions, specifically focusing on solvent tolerance in P. putida strains. The backbone of pTTS12 was found to be closely related to that of the carbapenem-resistance plasmid pOZ176, member of the IncP-2 incompatibility group, although the carbapenem resistance cassette is absent from pTTS12. Megaplasmid pTTS12 contains multiple transposon-flanked cassettes mediating resistance to various heavy metals such as tellurite, chromate (Tn7), and mercury (Tn5053 and Tn5563). Additionally, pTTS12 also contains a P-type, Type IV secretion system (T4SS) supporting self-transfer to other P. putida strains. This study increases our understanding in the modular structure of pTTS12 as a member of IncP-2 plasmid family and several promising exchangeable gene clusters to construct robust microbial hosts for biotechnology applications.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1001472/fullPseudomonas putidagenome sequencesolvent tolerancemegaplasmidmobile genetic elementscomparative analysis
spellingShingle Hadiastri Kusumawardhani
Hadiastri Kusumawardhani
Rohola Hosseini
Jo-Anne Verschoor
Johannes H. de Winde
Comparative analysis reveals the modular functional structure of conjugative megaplasmid pTTS12 of Pseudomonas putida S12: A paradigm for transferable traits, plasmid stability, and inheritance?
Frontiers in Microbiology
Pseudomonas putida
genome sequence
solvent tolerance
megaplasmid
mobile genetic elements
comparative analysis
title Comparative analysis reveals the modular functional structure of conjugative megaplasmid pTTS12 of Pseudomonas putida S12: A paradigm for transferable traits, plasmid stability, and inheritance?
title_full Comparative analysis reveals the modular functional structure of conjugative megaplasmid pTTS12 of Pseudomonas putida S12: A paradigm for transferable traits, plasmid stability, and inheritance?
title_fullStr Comparative analysis reveals the modular functional structure of conjugative megaplasmid pTTS12 of Pseudomonas putida S12: A paradigm for transferable traits, plasmid stability, and inheritance?
title_full_unstemmed Comparative analysis reveals the modular functional structure of conjugative megaplasmid pTTS12 of Pseudomonas putida S12: A paradigm for transferable traits, plasmid stability, and inheritance?
title_short Comparative analysis reveals the modular functional structure of conjugative megaplasmid pTTS12 of Pseudomonas putida S12: A paradigm for transferable traits, plasmid stability, and inheritance?
title_sort comparative analysis reveals the modular functional structure of conjugative megaplasmid ptts12 of pseudomonas putida s12 a paradigm for transferable traits plasmid stability and inheritance
topic Pseudomonas putida
genome sequence
solvent tolerance
megaplasmid
mobile genetic elements
comparative analysis
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1001472/full
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