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Lactiplantibacillus plantarum HB: A koumiss-derived Lactobacillus alleviates Toxoplasma gondii infection through regulating gut microbiota and metabolism

ABSTRACT:

Toxoplasma gondii (T. gondii) is an obligate intracellular protozoan parasite capable of infecting nearly all warm-blooded animals, including humans, with epidemiological studies indicating remarkably high global infection. However, due to its complex life cycle, no effective vaccine has been widely applied. Studies have revealed that many pathogen-induced infections can be mitigated by regulating the intestinal microenvironment. Probiotics, recognized as food-safe microbial agents for gut ecosystem modulation, have become a hotspot in developing novel interventions. Building upon our previous discovery that koumiss alleviates T. gondii infection in mice, this study successfully isolated Lactiplantibacillus plantarum HB (L. plantarum HB)-the most efficacious strain identified through screening from this koumiss, and further investigated its alleviative efficacy and mechanisms against toxoplasmosis. Results demonstrated that L. plantarum HB significantly ameliorated ileal inflammation and neuroinflammation, accompanied by marked reductions in parasite burden in multiple organs and brain tissues, while uncovering dynamic cytokine alterations during infection progression. Correlation analyses established direct associations between these alleviate outcomes and L. plantarum HB-mediated gut microbiota restructuring: acute-phase mitigation of ileal inflammation correlated with upregulated Akkermansia and downregulated Escherichia abundances, while chronic-phase neuroprotection was associated with enriched Lactobacillaceae and Bifidobacterium. Whole-genome sequencing revealed genetic determinants potentially underlying L. plantarum HB's functional, including carbohydrate metabolism and amino acid biosynthesis. Metabolomic profiling further elucidated alleviate mechanisms involving protein digestion and absorption, D-amino acid metabolism, and histidine metabolic regulation. These findings advance the understanding of probiotic applications and provide novel insights into mitigating toxoplasmosis.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase, Liquid Chromatography MS - positive - reverse phase

PROVIDER: MTBLS12987 | MetaboLights | 2025-09-12

REPOSITORIES: MetaboLights

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			Action	DRS
	a_MTBLS12987_LC-MS_negative_reverse-phase_metabolite_profiling.txt	Txt
	a_MTBLS12987_LC-MS_positive_reverse-phase_metabolite_profiling.txt	Txt
	i_Investigation.txt	Txt
	m_MTBLS12987_LC-MS_negative_reverse-phase_metabolite_profiling_v2_maf.tsv	Tabular
	m_MTBLS12987_LC-MS_positive_reverse-phase_metabolite_profiling_v2_maf.tsv	Tabular

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Project description:Toxoplasma gondii is an obligate intracellular parasite which can cause toxoplasmosis. Surface and secreted proteins of T. gondii play important roles in infection and immunity, and also are antigen targets in immunological diagnosis and vaccine development. However, it is difficult to investigate identities and antigenicities of surface and secreted proteins due to limitation of surface protein extraction methods. In this study, a total of 785 potential surface and secreted proteins of T. gondii RH tachyzoites were identified using a method combination of biotin labeling, avidin chromatography isolation, and high flux proteomics (LC-MS/MS). Among the highly-expressed 65 proteins, 43 proteins (66%) were originally annotated as surface or secreted proteins in the released T. gondii genomes, which proved the method combination to be a credible strategy. Furthermore, the transcriptomic responses and cytokine secretions induced by the isolated proteins, the live T. gondii RH tachyzoites infection, and the live pathogenic E. coli infection, in the human peripheral blood monocyte THP-1 cell lines, were comparatively analyzed to reveal antigenicities and immunobiological properties of T. gondii surface and secreted proteins. The transciptomic profiles induced by the isolated proteins were similar to those induced by the live bacterium infection, but were different from those induced by the live parasite infection. Contrary to the low cytokine secretion induced by the live parasite infection, the isolated proteins induced significant cytokine and chemokines secretion. Especially, the secretions of several chemokines induced by the isolated proteins were even higher than those induced by the live bacterium infection. These data suggested that T. gondii surface and secreted proteins were effective antigens, while the live parasite could evade the host innate immunity. This study comprehensively revealed the identities and antigenicities of T. gondii surface and secreted proteins, which laid foundation for further screening new T. gondii antigens, developing immunological diagnosis methods, and studying host immune response to T. gondii infection.

Project description:The innate immune response of mucosal epithelial cells during pathogen invasion plays a central role in immune regulation in the gut. Toxoplasma gondii (T. gondii) is a protozoan intracellular parasite that is usually transmitted through oral infection. Although much of the information on immunity to T. gondii has come from intra-peritoneal infection models, more recent studies have revealed the importance of studying immunity following infection through the natural per-oral route. Oral infection studies have identified many of the key players in the intestinal response; however, they have relied on responses detected days to weeks following infection. Much less is known about how the gut epithelial layer senses and reacts during initial contact with the pathogen. Given the importance of epithelial cells during pathogen invasion, this study uses an in vitro approach to isolate the key players and examine the early response of intestinal epithelial cells during infection by T. gondii. We show that human intestinal epithelial cells infected with T. gondii elicit rapid MAPK phosphorylation, NF-ÎºB nuclear translocation, and secretion of interleukin (IL)-8. Both ERK1/2 activation and IL-8 secretion responses were shown to be MyD88 dependent and TLR2 was identified to be involved in the recognition of the parasite regardless of the parasite genotype. Furthermore, we were able to identify additional T. gondii-regulated genes in the infected cells using a pathway-focused array. Together, our findings suggest that intestinal epithelial cells were able to recognize T. gondii during infection, and the outcome is important for modulating intestinal immune responses. Oral infection studies have demonstrated an increase in several cytokines and chemokines in response to T.gondii infection; however, the mixed population of the intestinal mucosa did not allow for the determination of the relative role that specific cell populations play in the production of these mediators. To address the role of intestinal epithelial cells to modulate the cytokine environment early following infection, we used specific pathway arrays to identify cytokines and chemokines induced 4 hours after exposure to T. gondii. At this time point most cells have become infected, but the parasites have not replicated.

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Lactiplantibacillus plantarum HB: A koumiss-derived Lactobacillus alleviates Toxoplasma gondii infection through regulating gut microbiota and metabolism

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