In vitro evaluation of the immunomodulatory and wakame assimilation properties of Lactiplantibacillus plantarum strains from swine milk

Ryusuke Ohgi; Sudeb Saha; Binghui Zhou; Taiga Sakuma; Mitsuki Sakurai; Yuhka Nakano; Fu Namai; Wakako Ikeda-Ohtsubo; Yoshihito Suda; Keita Nishiyama; Julio Villena; Haruki Kitazawa

doi:10.3389/fmicb.2024.1324999

In vitro evaluation of the immunomodulatory and wakame assimilation properties of Lactiplantibacillus plantarum strains from swine milk

Front Microbiol. 2024 Jan 26:15:1324999. doi: 10.3389/fmicb.2024.1324999. eCollection 2024.

Authors

Ryusuke Ohgi^#¹, Sudeb Saha^#^{1

2}, Binghui Zhou^{1

3}, Taiga Sakuma¹, Mitsuki Sakurai¹, Yuhka Nakano¹, Fu Namai^{1

3}, Wakako Ikeda-Ohtsubo^{1

3}, Yoshihito Suda⁴, Keita Nishiyama^{1

3}, Julio Villena^{1

5}, Haruki Kitazawa^{1

3}

Affiliations

¹ Food and Feed Immunology Group, Laboratory of Animal Food Function, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.
² Department of Dairy Science, Faculty of Veterinary, Animal and Biomedical Sciences, Sylhet Agricultural University, Sylhet, Bangladesh.
³ Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.
⁴ Department of Food Resource Development, School of Food Industrial Sciences, Miyagi University, Sendai, Japan.
⁵ Laboratory of Immunobiotechnology, Reference Centre for Lactobacilli (CERELA-CONICET), Tucuman, Argentina.

^# Contributed equally.

Abstract

The emergence and spread of antibiotic resistance threat forced to explore alternative strategies for improving the resistance to pathogens in livestock production. Probiotic lactic acid bacteria represent an alternative for this objective. In this study, seven Lactiplantibacillus plantarum strains from porcine colostrum and milk were isolated, identified and characterized in terms of their abilities to modulate immunity in porcine intestinal epithelial (PIE) cells. Then, two potential immunoregulatory strains were studied in terms of their ability to utilize and grow in wakame (Undaria pinnafida). Isolates were identified by 16S rRNA gene and evaluated by studying their interaction with PIE cells. The expressions of peptidoglycan recognition proteins (PGRPs), nucleotide-binding oligomerization domain (NODs), host defense peptides (pBD), and type I interferons (IFNs) were evaluated by RT-qPCR. The strain 4M₄417 showed a remarkable capacity to differentially regulate the expression of PGRP1, PGRP3, NOD1, NOD2, and pBD1 in PIE cells. On the other hand, the strain 4M₄326 was the most efficient to improve the expression of IFN-α and IFN-β in PIE cells challenged with poly (I:C). Both L. plantarum 4M₄326 and 4M₄417 were characterized in terms of their ability to utilize wakame. Results demonstrated that both strains efficiently grew in wakame-based broth. Our results suggest that L. planatrum 4M₄326 and 4M₄417 are interesting candidates to develop immunomodulatory feeds based on wakame utilization. These new immunosynbiotic feeds could help to reduce severity of intestinal infections and improve immune health status in pigs.

Keywords: Lactobacillus plantarum; immunomodulatory potential; pig milk; porcine intestinal epithelial cells; wakame.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by Grants-in-Aid for Scientific Research (A) (19H00965, 23H00354 HK), Grant-in-Aid for Scientific Research (B) (23H02358, KN), Grant-in-Aid for Early-Career Scientists (22K14982, BZ), Grant-in-Aid for Research Activity Start-up (23K19327, FN), and a Challenging Research (Exploratory, 23K18072, HK) and JSPS Fellows (22F22080, HK) from the Japan Society for the Promotion of Science (JSPS). This research was also supported by the Research Program on Development of Innovative Technology Grants (JPJ007097) from the Project of the Bio-Oriented Technology Research Advancement Institution (BRAIN) and by the Japan Racing Association to HK. This work was also supported by the JSPS Core-to-Core Program, A. Advanced Research Networks, entitled Establishment of International Agricultural Immunology Research Core for Quantum Improvement in Food Safety.