A comparative assessment of Lactiplantibacillus plantarum isolated from chicken and humans as candidates for probiotics
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Abstract. Sunardi J, Purnama ET, Sugata M, Victor H, Jan TT, Jo J. 2023. A comparative assessment of Lactiplantibacillus plantarum isolated from chicken and humans as candidates for probiotics. Biodiversitas 24: 5198-5206. Lactiplantibacillus plantarum is commonly analyzed as a potential probiotic. We hereby investigated two strains isolated from chicken crop (Lpb. plantarum F75) and human breast milk (Lpb. plantarum SU-KC1a). Ability to withstand osmotic stress (1.5%, 2.5% or 3.5% of NaCl) and phenol compounds (0.2% or 0.5%), ability to survive gastric juices for a maximum of 120 minutes and bile salt for a maximum 3 hours, as well as susceptibility to 25 antibiotic discs, were compared between both strains. Whole genomes of both strains were sequenced and analyzed in silico to determine the availability of antibiotic-resistance genes as well as the presence of mobile genetic elements and plasmid. Both strains were sensitive to increased concentrations of NaCl and phenol as well as to prolonged exposure to gastric juices. In contrast, both strains could withstand a prolonged exposure of 0.3% of bile salt. Both isolates had similar genome sizes and were susceptible to many tested antibiotics. The detected resistance genes were observed within the chromosomal genomes but no mobile genetic element nor plasmid was found. In conclusion, both strains of Lpb. plantarum displayed several characteristics of beneficial bacteria and could be used as probiotic candidates for poultry and human beings, respectively.
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References
Bigliardi B, Galati F. 2013. Innovation trends in the food industry: The case of functional foods. Trends in Food Science and Technology 31(2):118-129. DOI: https://doi.org/10.1016/j.tifs.2013.03.006.
Binda S, Hill C, Johansen E, Obis D, Pot B, Sanders ME, Tremblay A, Ouwerhand AC. 2020. Criteria to qualify microorganisms as “probiotic” in foods and dietary supplements. Frontiers in Microbiology 11:1662. DOI: https://doi.org/10.3389/fmicb.2020.01662.
Campedelli I, Mathur H, Salvetti E, Clarke S, Rea MC, Torriani S, Ross RP, Hill C, O’Toole PW. 2019. Genus-wide assessment of antibiotic resistance in Lactobacillus spp. Applied and Environmental Microbiology 85(1):e01738-01818. DOI: https://doi.org/10.1128/aem.01738-18.
Charteris WP, Kelly PM, Morelli L, Collins JK. 1998. Antibiotic susceptibility of potentially probiotic Lactobacillus species. Journal of Food Protection 61(12):1636-1643. DOI:10.4315/0362-028x-61.12.1636.
Chukiatsiri K, Sasipreeyajan J, Blackall PJ, Yuwatanichsampan S, Chansiripornchai N. 2012. Serovar identification, antimicrobial sensitivity, and virulence of avibacterium paragallinarum isolated from chickens in Thailand. Avian Disease 56(2):359-364. DOI: 10.1637/9881-080811-Reg.1.
Clinical and Laboratory Standards Institute. 2023. M100 performance standards for antimicrobial susceptibility testing 33rd Edition. http://em100.edaptivedocs.net/GetDoc.aspx?doc=CLSI%20M100%20ED33:2023&format=SPDF#DocTop
Das DJ, Shankar A, Johnson JB, Thomas S. 2020. Critical insights into antibiotic resistance transferability in probiotic Lactobacillus. Nutrition 69:110567. DOI: https://doi.org/10.1016/j.nut.2019.110567.
Dec M, Urban-Chmiel R, St?pie?-Py?niak D, Wernicki A. 2017. Assessment of antibiotic susceptibility in Lactobacillus isolates from chickens. Gut Pathogens 9(1):54. DOI: https://doi.org/10.1186/s13099-017-0203-z
Di Renzo L, Gualtieri P, Pivari F, Soldati L, Attinà A, Cinelli G, Leggeri C, Caparello G, Barrea L, Scerbo F, Esposito E, Lorenzo AD. 2020. Eating habits and lifestyle changes during COVID-19 lockdown: An Italian survey. Journal of Translational Medicine 18(1):229. DOI: https://doi.org/10.1186/s12967-020-02399-5.
Dikson, Victor H, Jong D, Sanjaya A, Samantha A, Jo J, R Pinontoan. 2022. Whole-genome analysis of Bacillus subtilis G8 isolated from natto. Biodiversitas 23(3):1293-1300. DOI: https://doi.org/10.13057/biodiv%2Fd230313.
Epi2Me. Assembly of Small Genomes. 2020. https://labs.epi2me.io/notebooks/Assembly_Tutorial.html
Fidanza M, Panigrahi P, Kollmann TR. 2021. Lactiplantibacillus plantarum–nomad and ideal probiotic. Frontiers in Microbiology 12:712236. DOI: https://doi.org/10.3389%2Ffmicb.2021.712236.
Filannino P, De Angelis M, Di Cagno R, Gozzi G, Riciputi Y, Gobbetti M. 2018. How Lactobacillus plantarum shapes its transcriptome in response to contrasting habitats. Environmental Microbiology 20(10):3700-3716. DOI: 10.1111/1462-2920.14372.
Filannino P, Di Cagno R, Crecchio C, De Virgilio C, De Angelis M, Gobbetti M. 2016. Transcriptional reprogramming and phenotypic switching associated with the adaptation of Lactobacillus plantarum C2 to plant niches. Scientific Reports 6: 27392. DOI: https://doi.org/10.1038/srep27392.
Floch N. 2017. The influence of microbiota on mechanisms of bariatric surgery. In: Floch MH, Ringel Y, Walker WA, (eds.). The Microbiota in Gastrointestinal Pathophysiology. Elsevier, Amsterdam.
Gu XC, Luo XG, Wang CX, Ma DY, Wang Y, He YY, Li W, Zhou H, Zhang TC. 2014. Cloning and analysis of bile salt hydrolase genes from Lactobacillus plantarum CGMCC No. 8198. Biotechnology Letters 36:975-983. DOI: 10.1007/s10529-013-1434-9
Heunis T, Deane S, Smit S, Dicks LM. 2014. Proteomic profiling of the acid stress response in Lactobacillus plantarum 423. Journal of Proteome Research 13(9):4028-4039. DOI: 10.1021/pr500353x
He Y, Lei J, Pan X, Huang X, Zhao Y. 2020. The hydrolytic water molecule of Class A ?-lactamase relies on the acyl-enzyme intermediate ES* for proper coordination and catalysis. Science Reports 10(1):10205. DOI: https://doi.org/10.1038/s41598-020-66431-w.
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli, L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME. 2014. Expert consensus document: The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology 11(8):506-514. DOI: https://doi.org/10.1038/nrgastro.2014.66.
Huang R, Pan M, Wan C, Shah NP, Tao X, Wei H. 2016. Physiological and transcriptional responses and cross protection of Lactobacillus plantarum ZDY2013 under acid stress. Journal of Dairy Science 99(2):1002-1010. DOI: 10.3168/jds.2015-9993.
Inglin RC, Meile L, Stevens MJA. 2018. Clustering of pan- and core-genome of Lactobacillus provides novel evolutionary insights for differentiation. BMC Genomics 19(1):284. DOI: https://doi.org/10.1186/s12864-018-4601-5
Jiang M, Zhang F, Wan C, Xiong Y, Shah NP, Wei H, Tao X. 2016. Evaluation of probiotic properties of Lactobacillus plantarum WLPL04 isolated from human breast milk. Journal of Dairy Science 99(3):1736-1746. DOI: https://doi.org/10.3168/jds.2015-10434.
Jorgensen JH, Turnidge JD. 2015. Susceptibility test methods: dilution and disk diffusion methods. In: Jorgensen JH, Carroll KC, Funke G, Pfaller MA, Landry ML, Richter SS, Warnock DW (eds.). Manual of Clinical Microbiology 11th Edition. Wiley, New Jersey.
Karaseva O, Ozhegov G, Khusnutdinova D, Siniagina M, Anisimova E, Akhatova F, Fakhrullin R, Yarullina D. 2023. Whole genome sequencing of the novel probiotic strain Lactiplantibacillus plantarum FCa3L. Microorganisms 11(5):1234. DOI: 10.3390/microorganisms11051234.
Li T, Teng D, Mao R, Hao Y, Wang X, Wang J. 2020. A critical review of antibiotic resistance in probiotic bacteria. Food Research International 136:109571. DOI: https://doi.org/10.1016/j.foodres.2020.109571.
Martino ME, Bayjanov JR, Caffrey BE, Wels M, Joncour P, Hughes S, Gillet B, Kleerebezem M, van Hijum SAFT, Leulier F. 2016. Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats. Environmental Microbiology 18(12):4974-4989. DOI: https://doi.org/10.1111/1462-2920.13455.
Mokoena MP. 2017. Lactic acid bacteria and their bacteriocins: Classification, biosynthesis and applications against uropathogens: A mini-review. Molecules 22(8):1255. DOI: https://doi.org/10.3390/molecules22081255.
Morrison DJ, Preston T. 2016. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7(3):189-200. DOI: https://doi.org/10.1080%2F19490976.2015.1134082.
Müller A, Hächler H, Stephan R, Lehner A. 2014. Presence of AmpC beta-lactamases, CSA-1, CSA-2, CMA-1, and CMA-2 conferring an unusual resistance phenotype in Cronobacter sakazakii and Cronobacter malonaticus. Microbial Drug Resistance 20(4):275-280. DOI: https://doi.org/10.1089/mdr.2013.0188.
National Library of Medicine. Genome List. 2023. https://www.ncbi.nlm.nih.gov/genome/browse#!/prokaryotes/1108/
Nature Medicine. 2023. Food as medicine: translating the evidence. Nature Medicine 29(4):753-4. DOI: https://doi.org/10.1038/s41591-023-02330-7
Okonechnikov K, Conesa A, García-Alcalde F. 2016. Qualimap 2: Advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 32(2):292-294. DOI: https://doi.org/10.1093/bioinformatics/btv566.
Pacheco-Ordaz R, Wall-Medrano A, Goñi MG, Ramos-Clamont-Montfort G, Ayala-Zavala JF, González-Aguilar GA. 2018. Effect of phenolic compounds on the growth of selected probiotic and pathogenic bacteria. Letters in Applied Microbiology 66(1):25-31. DOI: https://doi.org/10.1111/lam.12814.
Papadimitriou K, Alegria A, Brron PA, de Angelis M, Gobbetti M, Kleerebezem M, Lemos JA, Linares DM, Ross P, Stanton C, Turroni F, Sinderen D, Varmanen P, Ventura M, Zuniga M, Tsakalidou E, Kok J. 2016. Stress physiology of lactic acid bacteria. Microbiology and Molecular Biology Reviews 80(3):837-890. DOI: https://doi.org/10.1128%2FMMBR.00076-15.
Parlindungan E, Lugli GA, Ventura M, van Sinderen D, Mahony J. 2021. Lactic acid bacteria diversity and characterization of probiotic candidates in fermented meats. Foods 10(7):1519. DOI: https://doi.org/10.3390/foods10071519.
Peterson E, Kaur P. 2018. Antibiotic resistance mechanisms in bacteria: Relationships between resistance determinants of antibiotic producers, environmental bacteria, and clinical pathogens. Frontiers in Microbiology 9:2928. DOI: https://doi.org/10.3389/fmicb.2018.02928.
Rahman SJ, Kaur P. 2018. Conformational changes in a multidrug resistance ABC transporter DrrAB: Fluorescence-based approaches to study substrate binding. Archives of Biochemistry and Biophysics 658:31-45. DOI: https://doi.org/10.1016/j.abb.2018.09.017.
Rolain JM. 2013. Food and human gut as reservoirs of transferable antibiotic resistance encoding genes. Frontiers in Microbiology 4. DOI: https://doi.org/10.3389/fmicb.2013.00173.
Selim S. 2022. Mechanisms of gram-positive vancomycin resistance (Review). Biomedical Reports 16(1):7. DOI: https://doi.org/10.3892%2Fbr.2021.1490.
Seme H, Gjuracic K, Kos B, Fujs S, Stempelj M, Petkovic H, Suskovic J, Bogovic Matijasic B, Kosec G. 2015. Acid resistance and response to pH-induced stress in two Lactobacillus plantarum strains with probiotic potential. Beneficial Microbes 6(3):369-379. DOI: 10.3920/BM2014.0069.
Sharma C, Gulati S, Thakur N, Singh BP, Gupta S, Kaur S, Mishra SK, Puniya AK, Gill JPS, Panwar H. 2017. Antibiotic sensitivity pattern of indigenous lactobacilli isolated from curd and human milk samples. 3 Biotech 7(1):53. DOI: https://doi.org/10.1007/s13205-017-0682-0.
Silva YP, Bernardi A, Frozza RL. 2020. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Frontiers in Endocrinology 11:25. DOI: https://doi.org/10.3389/fendo.2020.00025.
Singh A, Kaur K, Mohana P, Kaur A, Kaur K, Heer S, Arora S, Bedi N, Bedi PMSB. 2021. Mechanistic insights of drug resistance in Staphylococcus aureus with special reference to newer antibiotics. In: Aqib A (eds.). Insights Into Drug Resistance in Staphylococcus aureus. IntechOpen, Vienna.
Stogios PJ, Savchenko A. 2020. Molecular mechanisms of vancomycin resistance. Protein Science 29:654-669. DOI: 10.1002/pro.3819.
Tamma PD, Doi Y, Bonomo RA, Johnson JK, Simner PJ. 2019. A primer on AmpC B-lactamases: necessary knowledge for an increasingly multidrug-resistant world. Clinical Infectious Disease 69(8):1446-1455. DOI: https://doi.org/10.1093/cid/ciz173.
Tanizawa Y, Fujisawa T, Nakamura Y. 2018. DFAST: A flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 34(6):1037-1039. DOI: https://doi.org/10.1093/bioinformatics/btx713.
Temple NJ. 2022. A rational definition for functional foods: A perspective. Frontier in Nutrition 9:957516. DOI: https://doi.org/10.3389/fnut.2022.957516.
Thananimit S, Pahumunto N, Teanpaisan R. 2022. Characterization of short chain fatty acids produced by selected potential probiotic Lactobacillus strains. Biomolecules 12(12):1829. DOI: https://doi.org/10.3390/biom12121829.
Valdés L, Cuervo A, Salazar N, Ruas-Madiedo P, Gueimonde M, González S. 2015. The relationship between phenolic compounds from diet and microbiota: Impact on human health. Food and Function 6(8):2424-2439. DOI: https://doi.org/10.1039/c5fo00322a.
Wang G, Yu H, Feng X, Tang H, Xiong Z, Xia Y, Ai L, Song X. 2021. Specific bile salt hydrolase genes in Lactobacillus plantarum AR113 and relationship with bile salt resistance. Lebensmittel-Wissenschaft+Technologie 145:111208. DOI: https://doi.org/10.1016/j.lwt.2021.111208.
Wattal C, Oberol JK. 2014. Mupirocin resistant Staphylococcus aureus nasal colonization among healthcare workers. Indian Journal of Critical Care Medicine 18(11):709-710. DOI: https://doi.org/10.4103%2F0972-5229.144009.
Yang Y, Liu Y, Zhou S, Huang L, Chen Y, Huan H. 2019. Bile salt hydrolase can improve Lactobacillus plantarum survival in gastrointestinal tract by enhancing their adhesion ability. FEMS Microbiology Letters 366(8):fnz100. DOI: https://doi.org/10.1093/femsle/fnz100.
Zheng L, Hu Y, He X, Zhao Y, Xu H. 2020. Isolation of swine?derived Lactobacillus plantarum and its synergistic antimicrobial and health?promoting properties with ZnO nanoparticles. Journal of Applied Microbiology 128(6):1764-1775. DOI: https://doi.org/10.1111/jam.14605.
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