Whole-Genome Analysis and Tolerance Assessment on Bifidobacteria-like Bacteria Isolated from Breast Milk and Infant Fecal Samples in Indonesia
Keywords:
Bifidobacterium species, Human Breast Milk, Infant Feces, Lactobacillus species, Probiotics, Whole Genome
Abstract
Probiotics are living microorganisms that can provide health benefits to the host when administered in sufficient quantities. To exert their health effects, probiotics must first be capable of surviving the harsh conditions of the gastrointestinal tract. We decided to sequence whole genomes of Bifidobacteria-like isolates (i.e., BS2-PS1, BS2-PS2, BS2-PB5, and BR2-12) and assess their abilities to resist low pH and bile salt. Molecular identification through whole genome sequencing indicated that the bacteria isolated from human breast milk were identified as Bifidobacterium breve (BS2-PS1 and BS2-PS2) and Lacticaseibacillus paracasei subspecies paracasei (BS2-PB5), whereas the bacteria isolated from infant feces was identified as Lactiplantibacillus plantarum (BR-12). All isolates exhibited resilience upon exposure to bile salts at concentrations of 0%, 0.3%, and 0.5%, with survival observed even at the highest concentration (0.5%) after three hours of incubation. The ability to withstand bile salt was presumably mediated by various genes that encode the resistance, e.g., bsh, cbh, dps, glf, cfa, or nagB, found in genomes of tested isolates. Upon exposure to pH 2 and 5 for three hours, BS2-PS1, BS2-PS2, and BR-12 exhibited acid resistance as well. The ability to withstand low pH could be mediated by the presence of relevant genes, e.g., argC, argH, dapA, pyk, pyrG, as well as genes that encode F0F1-ATPase enzyme, such as atpC, atpB, atpE, atpF, atpH, atpA, atpG, and atpD in their genomes. In summary, these results indicated the potential of all isolates to be further developed as probiotic candidates.
References
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Keffeler, E.C. et al., 2021. Metabolism of poly-Β1,4-n-acetylglucosamine substrates and importation of n-acetylglucosamine and glucosamine by Enterococcus faecalis. Journal of Bacteriology, 203(21). doi: 10.1128/jb.00371-21.
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Khushboo., Karnwal, A. & Malik, T., 2023. Characterization and selection of probiotic lactic acid bacteria from different dietary sources for development of Functional Foods. Frontiers in Microbiology, 14, pp.1–14. doi: 10.3389/fmicb.2023.1170725.
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Kingkaew, E. et al., 2023. Functional genome analysis and anti-helicobacter pylori activity of a novel bacteriocinogenic Lactococcus sp. NH2-7c from Thai fermented pork (NHAM). Scientific Reports, 13(1), pp.1–17. doi: 10.1038/s41598-023-47687-4.
Lawson, M.A.E. et al., 2020. Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem. The ISME Journal, 14(2), pp.635-648. doi: 10.1038/s41396-019-0553-2.
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Letunic, I. & Bork, P., 2021. Interactive tree of life (itol) V5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49(W1), pp.293–296. doi: doi.org/10.1093/nar/gkab301.
Marbun, K.T. et al., 2024. Genomic characterization and safety assessment of Bifidobacterium breve BS2- PB3 as functional food. Journal of Microbiology and Biotechnology, 34(4), pp.1-9. doi: 10.4014/jmb.2311.11031.
Martinez, I., Muller, C.E. & Walter, J., 2013. Long-term temporal analysis of the human fecal microbiota revealed a stable core of dominant bacterial species. PLoS ONE, 8(7), pp.69621. doi: 10.1371/journal.pone.0069621.
Meier-Kolthoff, J.P. & Göker, M., 2019. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nature Communications, 10(1), pp.194–225. doi: 10.1038/s41467-019-10210-3.
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Min, B. et al., 2022. Genomic characteristics and comparative genomic analysis of a probiotic bacterial strain, Lactiplantibacillus plantarum CKDB008. Food Supplements and Biomaterials for Health, 2(4), pp.1–20. doi: 10.52361/fsbh.2022.2.e32.
O’Flaherty, S. et al., 2018. The Lactobacillus bile salt hydrolase repertoire reveals niche-specific adaptation. mSphere, 3(3). doi: 10.1128/msphere.00140-18.
Ojo-Okunola, A., Nicol, M. & Toit, E., 2018. Human breast milk bacteriome in health and disease. Nutrients, 10(11), pp.1643–1656. doi: 10.3390/nu10111643.
Reyes-Castillo, P.A. et al., 2023. Bifidobacterium longum LBUX23 isolated from feces of a newborn; potential probiotic properties and genomic characterization. Microorganisms, 11(7), pp.1648–1667. doi: 10.3390/microorganisms11071648.
Rossi, F. et al., 2022. Variability of genetic characters associated with probiotic functions in Lacticaseibacillus species. Microorganisms, 10(5), pp.1023–1036. doi: 10.3390/microorganisms10051023.
Schöpping, M., Zeidan, A.A. & Franzén, C.J., 2022. Stress response in Bifidobacteria. Microbiology and Molecular Biology Reviews, 86(4). doi: 10.1128/mmbr.00170-21.
Shimizu, K. et al., 2023. Identification of genes essential for bile acid resistance in the probiotic Lacticaseibacillus paracasei strain Shirota. Letters in Applied Microbiology, 76(6). doi: 10.1093/lambio/ovad062.
Skoufou, M. et al., 2024. The networked interaction between probiotics and intestine in health and disease: A promising success story. Microorganisms, 12(1), pp,194–225. doi: 10.3390/microorganisms12010194.
Singhal, N. et al., 2021. Rhizospheric Lactiplantibacillus plantarum strains exhibit bile salt hydrolysis, hypocholestrolemic and probiotic capabilities in vitro. Scientific Reports, 11(1), pp.1–9. doi: 10.1038/s41598-021-94776-3.
Song, Z. et al., 2019. Taxonomic profiling and populational patterns of bacterial bile salt hydrolase (BSH) genes based on worldwide human gut microbiome. Microbiome, 7(1), pp.1-16. doi: 10.1186/s40168-019-0628-3.
Sunardi, J. et al., 2023. A comparative assessment of Lactiplantibacillus plantarum isolated from chicken and humans as candidates for probiotics. Biodiversitas Journal of Biological Diversity, 24(9) pp.5198-5206. doi: 10.13057/biodiv/d240964.
Tang, J. & Matsuda, Y., 2024. Discovery of fungal onoceroid triterpenoids through domainless enzyme-targeted global genome mining. Nature Communications, 15(1). doi: 10.1038/s41467-024-48771-7.
Tanizawa, Y. et al., 2016. DFAST and daga: Web-based Integrated Genome Annotation Tools and resources. Bioscience of Microbiota, Food and Health, 35(4), pp.173–184. doi: 10.12938/bmfh.16-003.
Tran, T.T.T. et al., 2021. Sulphate-reducing bacteria’s response to extreme pH environments and the effect of their activities on microbial corrosion. Applied Sciences, 11(5), pp.2201–2220. doi: 10.3390/app11052201.
Urdaneta, V. & Casadesús, J., 2017. Interactions between bacteria and bile salts in the gastrointestinal and hepatobiliary tracts. Frontiers in Medicine, 4(163), pp.1–13. doi: 10.3389/fmed.2017.00163.
Valdez-Baez, J. et al., 2022. Comparative genomics and in silico evaluation of genes related to the probiotic potential of Bifidobacterium breve 1101A. Bacteria, 1(3), pp.161–182. doi: 10.3390/bacteria1030013.
Vestergaard, M., Bald, D. & Ingmer, H., 2022. Targeting the ATP synthase in bacterial and fungal pathogens: Beyond Mycobacterium tuberculosis. Journal of Global Antimicrobial Resistance, 29, pp.29–41. doi: 10.1016/j.jgar.2022.01.026.
Virk, M.S. et al., 2024. The anti-inflammatory and curative exponent of probiotics: A comprehensive and authentic ingredient for the sustained functioning of major human organs. Nutrients, 16(4), pp.546–602. doi: 10.3390/nu16040546.
Wang, G. et al., 2021. Specific bile salt hydrolase genes in Lactobacillus plantarum AR113 and relationship with bile salt resistance. LWT, 145, pp.111208–111216. doi: 10.1016/j.lwt.2021.111208.
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Published
2025-04-11
How to Cite
Huang, T. F., Purnomo, J. S., Rombot, A. B., Kowanda, I. A., Lorentz, R. T., Sugata, M., Jan, T. T. and Jo, J. (2025) “Whole-Genome Analysis and Tolerance Assessment on Bifidobacteria-like Bacteria Isolated from Breast Milk and Infant Fecal Samples in Indonesia ”, Journal of Tropical Biodiversity and Biotechnology, 10(2), p. jtbb15062. doi: 10.22146/jtbb.15062.
Section
Research Articles
