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Metagenomic and metatranscriptomic profiling of Lactobacillus casei Zhang in the human gut.

ABSTRACT: Little is known about the replication and dynamic transcription of probiotics during their "passenger" journey in the human GI tract, which has therefore limited the understanding of their probiotic mechanisms. Here, metagenomic and metatranscriptomic sequencing was used to expose the in vivo expression patterns of the probiotic Lactobacillus casei Zhang (LcZ), which was compared with its in vitro growth transcriptomes, as well as the dynamics of the indigenous microbiome response to probiotic consumption. Extraction of the strain-specific reads revealed that replication and transcripts from the ingested LcZ were increased, while those from the resident L. casei strains remained unchanged. Mapping of all sequencing reads to LcZ genome showed that gene expression in vitro and in vivo differed dramatically. Approximately 39% of mRNAs and 45% of sRNAs of LcZ well-expressed were repressed after ingestion into human gut. The expression of ABC transporter genes and amino acid metabolism genes was induced at day 14 of ingestion, and genes for sugar and SCFA metabolism were activated at day 28 of ingestion. Expression of rli28c sRNA with peaked expression during the in vitro stationary phase was also activated in the human gut; this sRNA repressed LcZ growth and lactic acid production in vitro. However, the response of the human gut microbiome to LcZ was limited and heterogeneous. These findings implicate the ingested probiotic has to change its transcription patterns to survive and adapt in the human gut, and the time-dependent activation patterns indicate highly dynamic cross-talk between the probiotic and human gut microbes.

SUBMITTER: Wang J

PROVIDER: S-EPMC8249650 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The bacteriophage exclusion (BREX) system is a novel prokaryotic defense system against bacteriophages. To our knowledge, no study has systematically characterized the function of the BREX system in lactic acid bacteria. Lactobacillus casei Zhang is a probiotic bacterium originating from koumiss. By using single-molecule real-time sequencing, we previously identified N6-methyladenine (m6A) signatures in the genome of L. casei Zhang and a putative methyltransferase (MTase), namely, pglX This work further analyzed the genomic locus near the pglX gene and identified it as a component of the BREX system. To decipher the biological role of pglX, an L. casei Zhang pglX mutant (?pglX) was constructed. Interestingly, m6A methylation of the 5'-ACRCAG-3' motif was eliminated in the ?pglX mutant. The wild-type and mutant strains exhibited no significant difference in morphology or growth performance in de Man-Rogosa-Sharpe (MRS) medium. A significantly higher plasmid acquisition capacity was observed for the ?pglX mutant than for the wild type if the transformed plasmids contained pglX recognition sites (i.e., 5'-ACRCAG-3'). In contrast, no significant difference was observed in plasmid transformation efficiency between the two strains when plasmids lacking pglX recognition sites were tested. Moreover, the ?pglX mutant had a lower capacity to retain the plasmids than the wild type, suggesting a decrease in genetic stability. Since the Rebase database predicted that the L. casei PglX protein was bifunctional, as both an MTase and a restriction endonuclease, the PglX protein was heterologously expressed and purified but failed to show restriction endonuclease activity. Taken together, the results show that the L. casei Zhang pglX gene is a functional adenine MTase that belongs to the BREX system.IMPORTANCE Lactobacillus casei Zhang is a probiotic that confers beneficial effects on the host, and it is thus increasingly used in the dairy industry. The possession of an effective bacterial immune system that can defend against invasion of phages and exogenous DNA is a desirable feature for industrial bacterial strains. The bacteriophage exclusion (BREX) system is a recently described phage resistance system in prokaryotes. This work confirmed the function of the BREX system in L. casei and that the methyltransferase (pglX) is an indispensable part of the system. Overall, our study characterizes a BREX system component gene in lactic acid bacteria.

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Metagenomic and metatranscriptomic profiling of Lactobacillus casei Zhang in the human gut.

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