Control of Bacterial Phenotype and Chromosomal Gene Expression by Single Plasmids of <i>Lactococcus lactis</i> IL594

Plasmid-free <i>Lactococcus lactis</i> IL1403 is one of the best-characterized representatives of lactic acid bacteria (LAB), intensively used in broad microbiology worldwide. Its parent strain, <i>L. lactis</i> IL594, contains seven plasmids (pIL1–pIL7) with resolved DNA seq...

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Main Authors: Katarzyna Kosiorek, Anna Koryszewska-Bagińska, Marek Skoneczny, Tamara Aleksandrzak-Piekarczyk
Format: Article
Language:English
Published: MDPI AG 2023-06-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/12/9877
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author Katarzyna Kosiorek
Anna Koryszewska-Bagińska
Marek Skoneczny
Tamara Aleksandrzak-Piekarczyk
author_facet Katarzyna Kosiorek
Anna Koryszewska-Bagińska
Marek Skoneczny
Tamara Aleksandrzak-Piekarczyk
author_sort Katarzyna Kosiorek
collection DOAJ
description Plasmid-free <i>Lactococcus lactis</i> IL1403 is one of the best-characterized representatives of lactic acid bacteria (LAB), intensively used in broad microbiology worldwide. Its parent strain, <i>L. lactis</i> IL594, contains seven plasmids (pIL1–pIL7) with resolved DNA sequences and an indicated role for overall plasmid load in enhancing host-adaptive potential. To determine how individual plasmids manipulate the expression of phenotypes and chromosomal genes, we conducted global comparative phenotypic analyses combined with transcriptomic studies in plasmid-free <i>L. lactis</i> IL1403, multiplasmid <i>L. lactis</i> IL594, and its single-plasmid derivatives. The presence of pIL2, pIL4, and pIL5 led to the most pronounced phenotypic differences in the metabolism of several carbon sources, including some β-glycosides and organic acids. The pIL5 plasmid also contributed to increased tolerance to some antimicrobial compounds and heavy metal ions, especially those in the toxic cation group. Comparative transcriptomics showed significant variation in the expression levels of up to 189 chromosomal genes due to the presence of single plasmids and 435 unique chromosomal genes that were resultant of the activity of all plasmids, which may suggest that the observed phenotypic changes are not only the result of a direct action of their own genes but also originate from indirect actions through crosstalk between plasmids and the chromosome. The data obtained here indicate that plasmid maintenance leads to the development of important mechanisms of global gene regulation that provide changes in the central metabolic pathways and adaptive properties of <i>L. lactis</i> and suggest the possibility of a similar phenomenon among other groups of bacteria.
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spelling doaj.art-46061e65c74a4de78670101ad84dc7bf2023-11-18T10:45:24ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-06-012412987710.3390/ijms24129877Control of Bacterial Phenotype and Chromosomal Gene Expression by Single Plasmids of <i>Lactococcus lactis</i> IL594Katarzyna Kosiorek0Anna Koryszewska-Bagińska1Marek Skoneczny2Tamara Aleksandrzak-Piekarczyk3Institute of Biochemistry and Biophysics, Polish Academy of Sciences (IBB PAS), Pawińskiego 5a, 02-106 Warsaw, PolandDepartment of Medical Biology, Medical University of Warsaw, Litewska 14/16, 00-575 Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences (IBB PAS), Pawińskiego 5a, 02-106 Warsaw, PolandInstitute of Biochemistry and Biophysics, Polish Academy of Sciences (IBB PAS), Pawińskiego 5a, 02-106 Warsaw, PolandPlasmid-free <i>Lactococcus lactis</i> IL1403 is one of the best-characterized representatives of lactic acid bacteria (LAB), intensively used in broad microbiology worldwide. Its parent strain, <i>L. lactis</i> IL594, contains seven plasmids (pIL1–pIL7) with resolved DNA sequences and an indicated role for overall plasmid load in enhancing host-adaptive potential. To determine how individual plasmids manipulate the expression of phenotypes and chromosomal genes, we conducted global comparative phenotypic analyses combined with transcriptomic studies in plasmid-free <i>L. lactis</i> IL1403, multiplasmid <i>L. lactis</i> IL594, and its single-plasmid derivatives. The presence of pIL2, pIL4, and pIL5 led to the most pronounced phenotypic differences in the metabolism of several carbon sources, including some β-glycosides and organic acids. The pIL5 plasmid also contributed to increased tolerance to some antimicrobial compounds and heavy metal ions, especially those in the toxic cation group. Comparative transcriptomics showed significant variation in the expression levels of up to 189 chromosomal genes due to the presence of single plasmids and 435 unique chromosomal genes that were resultant of the activity of all plasmids, which may suggest that the observed phenotypic changes are not only the result of a direct action of their own genes but also originate from indirect actions through crosstalk between plasmids and the chromosome. The data obtained here indicate that plasmid maintenance leads to the development of important mechanisms of global gene regulation that provide changes in the central metabolic pathways and adaptive properties of <i>L. lactis</i> and suggest the possibility of a similar phenomenon among other groups of bacteria.https://www.mdpi.com/1422-0067/24/12/9877<i>Lactococcus lactis</i> IL594<i>L. lactis</i> IL1403plasmidsingle-plasmid derivativephenotypic and transcriptomic microarrays
spellingShingle Katarzyna Kosiorek
Anna Koryszewska-Bagińska
Marek Skoneczny
Tamara Aleksandrzak-Piekarczyk
Control of Bacterial Phenotype and Chromosomal Gene Expression by Single Plasmids of <i>Lactococcus lactis</i> IL594
International Journal of Molecular Sciences
<i>Lactococcus lactis</i> IL594
<i>L. lactis</i> IL1403
plasmid
single-plasmid derivative
phenotypic and transcriptomic microarrays
title Control of Bacterial Phenotype and Chromosomal Gene Expression by Single Plasmids of <i>Lactococcus lactis</i> IL594
title_full Control of Bacterial Phenotype and Chromosomal Gene Expression by Single Plasmids of <i>Lactococcus lactis</i> IL594
title_fullStr Control of Bacterial Phenotype and Chromosomal Gene Expression by Single Plasmids of <i>Lactococcus lactis</i> IL594
title_full_unstemmed Control of Bacterial Phenotype and Chromosomal Gene Expression by Single Plasmids of <i>Lactococcus lactis</i> IL594
title_short Control of Bacterial Phenotype and Chromosomal Gene Expression by Single Plasmids of <i>Lactococcus lactis</i> IL594
title_sort control of bacterial phenotype and chromosomal gene expression by single plasmids of i lactococcus lactis i il594
topic <i>Lactococcus lactis</i> IL594
<i>L. lactis</i> IL1403
plasmid
single-plasmid derivative
phenotypic and transcriptomic microarrays
url https://www.mdpi.com/1422-0067/24/12/9877
work_keys_str_mv AT katarzynakosiorek controlofbacterialphenotypeandchromosomalgeneexpressionbysingleplasmidsofilactococcuslactisiil594
AT annakoryszewskabaginska controlofbacterialphenotypeandchromosomalgeneexpressionbysingleplasmidsofilactococcuslactisiil594
AT marekskoneczny controlofbacterialphenotypeandchromosomalgeneexpressionbysingleplasmidsofilactococcuslactisiil594
AT tamaraaleksandrzakpiekarczyk controlofbacterialphenotypeandchromosomalgeneexpressionbysingleplasmidsofilactococcuslactisiil594