Comparative genome analysis of the immunomodulatory ability of Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from Japanese pickles
ABSTRACT Lactic acid bacteria (LAB) are pivotal in food preservation and exhibit immunomodulatory effects on interleukin-10 (IL-10) and interleukin-12 (IL-12) production. Lactiplantibacillus plantarum (L. plantarum) and Lactiplantibacillus pentosus (L. pentosus) from fermented food are known for the...
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American Society for Microbiology
2025-05-01
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| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01575-24 |
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| author | Yiting Liu Kazunori Sawada Takahiko Adachi Yuta Kino Tingyu Yin Naoyuki Yamamoto Takuji Yamada |
| author_facet | Yiting Liu Kazunori Sawada Takahiko Adachi Yuta Kino Tingyu Yin Naoyuki Yamamoto Takuji Yamada |
| author_sort | Yiting Liu |
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| description | ABSTRACT Lactic acid bacteria (LAB) are pivotal in food preservation and exhibit immunomodulatory effects on interleukin-10 (IL-10) and interleukin-12 (IL-12) production. Lactiplantibacillus plantarum (L. plantarum) and Lactiplantibacillus pentosus (L. pentosus) from fermented food are known for their effect; however, a comprehensive comparative genome analysis is needed to identify the linked genes. Here, we investigated the immunomodulatory capability at the genome level of L. plantarum and L. pentosus strains isolated from Japanese pickles at the genome level, and we further identified their immunomodulation-associated genes using the potential-gene (PG) index derived from the Calinski–Harabasz (CH) index. The results revealed an immunostimulatory clade with strain-specific IL-10 and IL-12 induction and identified key genes via the PG index. Both genes across two species were shown to encode the enzyme TagF2, which is crucial for synthesizing poly-glycerol-3-phosphate type wall teichoic acid (poly-GroP WTA), indicating that TagF2 plays a potential role as an effective microbe-associated-molecular-pattern. In vivo analyses confirmed the IL-10-inducing ability of one strain, reinforcing the IL-10-stimulating capacity of its poly-GroP WTA. Subpotential genes in L. plantarum TagF2-possessing strains were linked to host‒cell interactions, suggesting that such strains play potential probiotic roles. Collectively, the PG index effectively identified immunomodulation-related genes, thus paving the way for the use of the PG index to detect potential health benefit-associated genes in other LAB species.IMPORTANCELactic acid bacteria are pivotal in food preservation and exhibit immunomodulatory effects on interleukin-10 (IL-10) and interleukin-12 (IL-12) production. Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from fermented food are known for such effect, yet comprehensive comparative genome analysis is needed to elucidate the linked genes of the two species. The significance of our research is in observing the immunostimulatory clade with strain-specific cytokine induction and identifying key immunostimulation-related genes encoding enzymes that are crucial for synthesizing a potentially effective microbe-associated-molecular-pattern using the potential-gene index across two species. The further in vivo validation reinforced the interleukin-10-stimulating capacity of the identified pattern, and the detected sub-potential genes in Lactiplantibacillus plantarum key-gene possessing strains implied the utility of potential-gene index in detecting potential health-benefit-associated genes in other lactic acid bacteria species. |
| format | Article |
| id | doaj-art-cd8a67c6d24a4b80a7c4bef5eafcf168 |
| institution | OA Journals |
| issn | 2379-5077 |
| language | English |
| publishDate | 2025-05-01 |
| publisher | American Society for Microbiology |
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| spelling | doaj-art-cd8a67c6d24a4b80a7c4bef5eafcf1682025-08-20T01:52:31ZengAmerican Society for MicrobiologymSystems2379-50772025-05-0110510.1128/msystems.01575-24Comparative genome analysis of the immunomodulatory ability of Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from Japanese picklesYiting Liu0Kazunori Sawada1Takahiko Adachi2Yuta Kino3Tingyu Yin4Naoyuki Yamamoto5Takuji Yamada6School of Life Science and Technology, Institute of Science Tokyo, Tokyo, JapanInnovation Division, Gurunavi, Inc., Tokyo, JapanDepartment of Precision Health, Medical Research Institute, The Institute of Medical Engineering, Institute of New Industry Incubation, Institute of Science Tokyo, Tokyo, JapanSchool of Life Science and Technology, Institute of Science Tokyo, Tokyo, JapanSchool of Life Science and Technology, Institute of Science Tokyo, Tokyo, JapanSchool of Life Science and Technology, Institute of Science Tokyo, Tokyo, JapanSchool of Life Science and Technology, Institute of Science Tokyo, Tokyo, JapanABSTRACT Lactic acid bacteria (LAB) are pivotal in food preservation and exhibit immunomodulatory effects on interleukin-10 (IL-10) and interleukin-12 (IL-12) production. Lactiplantibacillus plantarum (L. plantarum) and Lactiplantibacillus pentosus (L. pentosus) from fermented food are known for their effect; however, a comprehensive comparative genome analysis is needed to identify the linked genes. Here, we investigated the immunomodulatory capability at the genome level of L. plantarum and L. pentosus strains isolated from Japanese pickles at the genome level, and we further identified their immunomodulation-associated genes using the potential-gene (PG) index derived from the Calinski–Harabasz (CH) index. The results revealed an immunostimulatory clade with strain-specific IL-10 and IL-12 induction and identified key genes via the PG index. Both genes across two species were shown to encode the enzyme TagF2, which is crucial for synthesizing poly-glycerol-3-phosphate type wall teichoic acid (poly-GroP WTA), indicating that TagF2 plays a potential role as an effective microbe-associated-molecular-pattern. In vivo analyses confirmed the IL-10-inducing ability of one strain, reinforcing the IL-10-stimulating capacity of its poly-GroP WTA. Subpotential genes in L. plantarum TagF2-possessing strains were linked to host‒cell interactions, suggesting that such strains play potential probiotic roles. Collectively, the PG index effectively identified immunomodulation-related genes, thus paving the way for the use of the PG index to detect potential health benefit-associated genes in other LAB species.IMPORTANCELactic acid bacteria are pivotal in food preservation and exhibit immunomodulatory effects on interleukin-10 (IL-10) and interleukin-12 (IL-12) production. Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from fermented food are known for such effect, yet comprehensive comparative genome analysis is needed to elucidate the linked genes of the two species. The significance of our research is in observing the immunostimulatory clade with strain-specific cytokine induction and identifying key immunostimulation-related genes encoding enzymes that are crucial for synthesizing a potentially effective microbe-associated-molecular-pattern using the potential-gene index across two species. The further in vivo validation reinforced the interleukin-10-stimulating capacity of the identified pattern, and the detected sub-potential genes in Lactiplantibacillus plantarum key-gene possessing strains implied the utility of potential-gene index in detecting potential health-benefit-associated genes in other lactic acid bacteria species.https://journals.asm.org/doi/10.1128/msystems.01575-24fermentationlactic acid bacteriacomparative genome analysisimmunomodulationglycerol wall teichoic acid |
| spellingShingle | Yiting Liu Kazunori Sawada Takahiko Adachi Yuta Kino Tingyu Yin Naoyuki Yamamoto Takuji Yamada Comparative genome analysis of the immunomodulatory ability of Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from Japanese pickles mSystems fermentation lactic acid bacteria comparative genome analysis immunomodulation glycerol wall teichoic acid |
| title | Comparative genome analysis of the immunomodulatory ability of Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from Japanese pickles |
| title_full | Comparative genome analysis of the immunomodulatory ability of Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from Japanese pickles |
| title_fullStr | Comparative genome analysis of the immunomodulatory ability of Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from Japanese pickles |
| title_full_unstemmed | Comparative genome analysis of the immunomodulatory ability of Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from Japanese pickles |
| title_short | Comparative genome analysis of the immunomodulatory ability of Lactiplantibacillus plantarum and Lactiplantibacillus pentosus from Japanese pickles |
| title_sort | comparative genome analysis of the immunomodulatory ability of lactiplantibacillus plantarum and lactiplantibacillus pentosus from japanese pickles |
| topic | fermentation lactic acid bacteria comparative genome analysis immunomodulation glycerol wall teichoic acid |
| url | https://journals.asm.org/doi/10.1128/msystems.01575-24 |
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