Marine Pediococcus pentosaceus E3 Probiotic Properties, Whole-Genome Sequence Analysis, and Safety Assessment.

Pediococcus pentosaceus Bacteriocin Comparative genomics Probiotic Safety

Journal

Probiotics and antimicrobial proteins

ISSN: 1867-1314

Titre abrégé: Probiotics Antimicrob Proteins

Pays: United States

ID NLM: 101484100

Informations de publication

Date de publication:
15 May 2024

Historique:

accepted: 01 05 2024

medline: 15 5 2024

pubmed: 15 5 2024

entrez: 15 5 2024

Statut: aheadofprint

Résumé

Probiotics play a significant role in enhancing health, and they are well known for bacteriocins production. Evaluating probiotics' whole-genome sequence provides insights into their consumption outcomes. Thus, genomic studies have a significant role in assessing the safety of probiotics more in-depth and offer valuable information regarding probiotics' functional diversity, metabolic pathways, and health-promoting mechanisms. Marine Pediococcus pentosaceus E3, isolated from shrimp gut, exhibited beneficial properties, indicating its potential as a probiotic candidate. Phenotypically, E3 strain was susceptible to most antibiotics assessed, tolerant to low pH and high bile salt conditions, and revealed no hemolysin activity. Interestingly, E3-neutralized CFS revealed significant antibacterial activity against pathogens under investigation. Therefore, the concentrated CFS was prepared and evaluated as a natural biopreservative and showed outstanding antimicrobial activity. Furthermore, integrated-based genome assessment has provided insight into probiotic characteristics at the genomic level. Whole-genome sequencing analysis revealed that the E3 genome possesses 1805 protein-coding genes, and the genome size was about 1.8 Mb with a G + C content of 37.28%. Moreover, the genome revealed the absence of virulence factors and clinically related antibiotic genes. Moreover, several genes consistent with probiotic microorganisms' features were estimated in the genome, including stress response, carbohydrate metabolism, and vitamin biosynthesis. In addition, several genes associated with survival and colonization within the gastrointestinal tract were also detected across the E3 genome. Therefore, the findings suggest that insights into the genetic characteristics of E3 guarantee the safety of the strain and facilitate future development of E3 isolate as a health-promoting probiotic and source of biopreservative.

Identifiants

DOI: 10.1007/s12602-024-10283-7 PMID: 38748306

pubmed: 38748306

doi: 10.1007/s12602-024-10283-7

pii: 10.1007/s12602-024-10283-7

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Informations de copyright

Références

Oh YJ, Kim SA, Yang SH et al (2022) Integrated genome-based assessment of safety and probiotic characteristics of Lactiplantibacillus plantarum PMO 08 isolated from kimchi. PLoS One 17(10):e0273986. https://doi.org/10.1371/journal.pone.0273986

doi: 10.1371/journal.pone.0273986 pubmed: 36190947 pmcid: 9529155

Kathiriya MR, Vekariya YV, Hati S (2023) Understanding the probiotic bacterial responses against various stresses in food matrix and gastrointestinal tract: a review. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-023-10104-3.10.1007/s12602-023-10104-3

doi: 10.1007/s12602-023-10104-3.10.1007/s12602-023-10104-3 pubmed: 37347421

Tegegne BA, Kebede B (2022) Probiotics, their prophylactic and therapeutic applications in human health development: a review of the literature. Heliyon 8(6):e09725. https://doi.org/10.1016/j.heliyon.2022.e09725

doi: 10.1016/j.heliyon.2022.e09725 pubmed: 35785237 pmcid: 9240980

Stavropoulou E, Bezirtzoglou E (2020) Probiotics in medicine: a long debate. Front Immunol. 11:2192. https://doi.org/10.3389/fimmu.2020.02192

doi: 10.3389/fimmu.2020.02192 pubmed: 33072084 pmcid: 7544950

Favaro L, Campanaro S, Fugaban JII et al (2023) Genomic, metabolomic, and functional characterisation of beneficial properties of Pediococcus pentosaceusST58, isolated from human oral cavity. Benef Microbes 14(1):57–72. https://doi.org/10.3920/BM2022.0067

doi: 10.3920/BM2022.0067 pubmed: 36815495

Capozzi V, Russo P, Dueñas MT, López P, Spano G (2012) Lactic acid bacteria producing B-group vitamins: a great potential for functional cereals products. Appl Microbiol Biotechnol 96(6):1383–1394. https://doi.org/10.1007/s00253-012-4440-2

doi: 10.1007/s00253-012-4440-2 pubmed: 23093174

Salazar N, Gueimonde M, de Los Reyes-Gavilán CG, Ruas-Madiedo P (2016) Exopolysaccharides produced by lactic acid bacteria and bifidobacteria as fermentable substrates by the intestinal microbiota. Crit Rev Food Sci Nutr 56(9):1440–1453. https://doi.org/10.1080/10408398.2013.770728

doi: 10.1080/10408398.2013.770728 pubmed: 25675369

Rozhkova IV, Yurova EA, Leonova VA (2023) Evaluation of the amino acid composition and content of organic acids of complex postbiotic substances obtained on the basis of metabolites of probiotic bacteria Lacticaseibacillus paracasei ABK and Lactobacillus helveticus H9. Fermentation 9(5):460. https://doi.org/10.3390/fermentation9050460

doi: 10.3390/fermentation9050460

Chen T, Wang L, Li Q et al (2020) Functional probiotics of lactic acid bacteria from Hu sheep milk. BMC Microbiol 20(1):228. https://doi.org/10.1186/s12866-020-01920-6

doi: 10.1186/s12866-020-01920-6 pubmed: 32723292 pmcid: 7390111

Qi Y, Huang L, Zeng Y et al (2021) Pediococcus pentosaceus: screening and application as probiotics in food processing. Front Microbiol 12:762467. https://doi.org/10.3389/fmicb.2021.762467

doi: 10.3389/fmicb.2021.762467 pubmed: 34975787 pmcid: 8716948

Zhao X, Higashikawa F, Noda M et al (2012) The obesity and fatty liver are reduced by plant-derived Pediococcus pentosaceus LP28 in high fat diet-induced obese mice. PLoS ONE 7(2):e30696. https://doi.org/10.1371/journal.pone.0030696

doi: 10.1371/journal.pone.0030696 pubmed: 22363472 pmcid: 3281851

Thirabunyanon M, Hongwittayakorn P (2013) Potential probiotic lactic acid bacteria of human origin induce antiproliferation of colon cancer cells via synergic actions in adhesion to cancer cells and short-chain fatty acid bioproduction. Appl Biochem Biotechnol 169(2):511–525. https://doi.org/10.1007/s12010-012-9995-y

doi: 10.1007/s12010-012-9995-y pubmed: 23239414

Sellamani M, Kalagatur NK, Siddaiah C et al (2016) Antifungal and zearalenone inhibitory activity of Pediococcus pentosaceus isolated from dairy products on Fusarium graminearum. Front Microbiol 7:890. https://doi.org/10.3389/fmicb.2016.00890

doi: 10.3389/fmicb.2016.00890 pubmed: 27379035 pmcid: 4904835

Kim JS, Kim JH, Palaniyandi SA et al (2019) Yak-Kong Soybean (Glycine max) Fermented by a novel Pediococcus pentosaceus inhibits the oxidative stress-induced monocyte-endothelial cell adhesion. Nutrients 11(6):1380. https://doi.org/10.3390/nu11061380

doi: 10.3390/nu11061380 pubmed: 31248152 pmcid: 6627370

Oliveira FS, da Silva RR, de Carvalho AF, Nero LA (2023) Genomic analyses of Pediococcus pentosaceus ST65ACC, a bacteriocinogenic strain Isolated from artisanal raw-milk cheese. Probiotics and Antimicrobial Proteins 15(3):630–645. https://doi.org/10.1007/s12602-021-09894-1

doi: 10.1007/s12602-021-09894-1 pubmed: 34984631

Choi GH, Fugaban JII, Dioso CM, Bucheli JEV, Holzapfel WH, Todorov SD (2023) Antimicrobial peptides (Bacteriocins) produced by Lactococcus lactis and Pediococcus pentosaceus strains with activity against clinical and food-borne pathogens. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-023-10188-x

doi: 10.1007/s12602-023-10188-x pubmed: 38064160

Kiousi DE, Rathosi M, Tsifintaris M, Chondrou P, Galanis A (2021) Pro-biomics: omics technologies to unravel the role of probiotics in health and disease. Adv Nutr 12(5):1802–1820. https://doi.org/10.1093/advances/nmab014

doi: 10.1093/advances/nmab014 pubmed: 33626128 pmcid: 8483974

Kiousi DE, Efstathiou C, Tegopoulos K et al (2022) Genomic insight into Lacticaseibacillus paracasei SP5, reveals genes and gene clusters of probiotic interest and biotechnological potential. Front Microbiol 13:922689. https://doi.org/10.3389/fmicb.2022.922689

doi: 10.3389/fmicb.2022.922689 pubmed: 35783439 pmcid: 9244547

Zaghloul HAH, El Halfawy NM (2022) Genomic insights into antibiotic-resistance and virulence genes of Enterococcus faecium strains from the gut of Apis mellifera. Microb Genom 8(11):mgen000896. https://doi.org/10.1099/mgen.0.000896

doi: 10.1099/mgen.0.000896 pubmed: 36374179 pmcid: 9836096

Wang Y, Liang Q, Lu B et al (2021) Whole-genome analysis of probiotic product isolates reveals the presence of genes related to antimicrobial resistance, virulence factors, and toxic metabolites, posing potential health risks. BMC Genomics 22(1):210. https://doi.org/10.1186/s12864-021-07539-9

doi: 10.1186/s12864-021-07539-9 pubmed: 33761872 pmcid: 7988973

Stergiou OS, Tegopoulos K, Kiousi DE et al (2021) Whole-genome sequencing, phylogenetic and genomic analysis of Lactiplantibacillus pentosus L33, a potential probiotic strain isolated from fermented sausages. Front Microbiol 12:746659. https://doi.org/10.3389/fmicb.2021.746659

doi: 10.3389/fmicb.2021.746659 pubmed: 34764945 pmcid: 8576124

El Sakkaa SE, Zaghloul EH, Ghanem KM (2022) Psychobiotic potential of gamma-aminobutyric acid-producing marine Enterococcus faecium SH9 from marine shrimp. Probiotics Antimicrob Proteins 14(5):934–946. https://doi.org/10.1007/s12602-022-09963-z

doi: 10.1007/s12602-022-09963-z pubmed: 35750975 pmcid: 9474364

Zaghloul EH, Abuohashish HM, El Sharkawy AS, Abbas EM, Ahmed MM, Al-Rejaie SS (2023) Probiotic potential of the marine isolate Enterococcus faecium EA9 and in vivo evaluation of its antisepsis action in rats. Mar Drugs 21(1):45. https://doi.org/10.3390/md21010045

doi: 10.3390/md21010045 pubmed: 36662218 pmcid: 9860781

Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069. https://doi.org/10.1093/bioinformatics/btu153

doi: 10.1093/bioinformatics/btu153 pubmed: 24642063

Wattam AR, Abraham D, Dalay O et al (2014) PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res 42(Database issue):D581–D591

doi: 10.1093/nar/gkt1099 pubmed: 24225323

Tatusova T, DiCuccio M, Badretdin A et al (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44(14):6614–6624. https://doi.org/10.1093/nar/gkw569

doi: 10.1093/nar/gkw569 pubmed: 27342282 pmcid: 5001611

Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428(4):726–731. https://doi.org/10.1016/j.jmb.2015.11.006

doi: 10.1016/j.jmb.2015.11.006 pubmed: 26585406

Dereeper A, Guignon V, Blanc G et al (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 1:36. https://doi.org/10.1093/nar/gkn180

doi: 10.1093/nar/gkn180

McArthur AG, Waglechner N, Nizam F et al (2013) The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57(7):3348–3357. https://doi.org/10.1128/AAC.00419-13

doi: 10.1128/AAC.00419-13 pubmed: 23650175 pmcid: 3697360

Arndt D, Grant JR, Marcu A et al (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44(W1):W16–W21. https://doi.org/10.1093/nar/gkw387

doi: 10.1093/nar/gkw387 pubmed: 27141966 pmcid: 4987931

Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34(Database issue):D32–D36. https://doi.org/10.1093/nar/gkj014

doi: 10.1093/nar/gkj014 pubmed: 16381877

Cosentino S, Voldby Larsen M, Møller Aarestrup F, Lund O (2013) PathogenFinder--distinguishing friend from foe using bacterial whole genome sequence data [published correction appears in PLoS One. 8(12). https://doi.org/10.1371/annotation/b84e1af7-c127-45c3-be22-76abd977600f ]. PLoS One. 2013;8(10):e77302. https://doi.org/10.1371/journal.pone.0077302

Zhang H, Yohe T, Huang L et al (2018) dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46(W1):W95–W101. https://doi.org/10.1093/nar/gky41

doi: 10.1093/nar/gky41 pubmed: 29771380 pmcid: 6031026

van Heel AJ, de Jong A, Song C, Viel JH, Kok J, Kuipers OP (2018) BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res 46(W1):W278–W281. https://doi.org/10.1093/nar/gky383

doi: 10.1093/nar/gky383 pubmed: 29788290 pmcid: 6030817

Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2016) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32(6):929–931. https://doi.org/10.1093/bioinformatics/btv681

doi: 10.1093/bioinformatics/btv681 pubmed: 26576653

Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5(6):e11147. https://doi.org/10.1371/journal.pone.0011147

doi: 10.1371/journal.pone.0011147 pubmed: 20593022 pmcid: 2892488

El Oirdi S, Tarik L, Ali AB, Meriem Y, Zouhair R, Abdelhaq B (2021) Isolation and identification of Lactobacillus plantarum 4F, a strain with high antifungal activity, fungicidal effect, and biopreservation properties of food.". J Food Process Preserv 45(6):e15517. https://doi.org/10.1111/jfpp.15517

doi: 10.1111/jfpp.15517

doi: 10.1016/j.heliyon.2022.e09725 pubmed: 35785237 pmcid: 9240980

Khushboo, Karnwal A, Malik T (2023) Characterization and selection of probiotic lactic acid bacteria from different dietary sources for development of functional foods. Front Microbiol 14:1170725. https://doi.org/10.3389/fmicb.2023.1170725

Merenstein D, Pot B, Leyer G et al (2023) Emerging issues in probiotic safety: 2023 perspectives. Gut Microbes 15(1):2185034. https://doi.org/10.1080/19490976.2023.2185034

doi: 10.1080/19490976.2023.2185034 pubmed: 36919522 pmcid: 10026873

Wanna W, Surachat K, Kaitimonchai P, Phongdara A (2021) Evaluation of probiotic characteristics and whole genome analysis of Pediococcus pentosaceus MR001 for use as probiotic bacteria in shrimp aquaculture. Sci Rep 11(1):18334. https://doi.org/10.1038/s41598-021-96780-z

doi: 10.1038/s41598-021-96780-z pubmed: 34526534 pmcid: 8443617

Oliveira FS, da Silva RR, de Carvalho AF, Nero LA (2023) Genomic analyses of Pediococcus pentosaceus ST65ACC, a bacteriocinogenic strain isolated from artisanal raw-milk cheese. Probiotics Antimicrob Proteins 15(3):630–645. https://doi.org/10.1007/s12602-021-09894-1

doi: 10.1007/s12602-021-09894-1 pubmed: 34984631

Drissi F, Merhej V, Angelakis E et al (2014) Comparative genomics analysis of Lactobacillus species associated with weight gain or weight protection. Nutr Diabetes 4(2):e109. https://doi.org/10.1038/nutd.2014.6

doi: 10.1038/nutd.2014.6 pubmed: 24567124 pmcid: 3940830

Diguță CF, Nițoi GD, Matei F, Luță G, Cornea CP (2020) The biotechnological potential of Pediococcus spp. isolated from Kombucha Microbial Consortium. Foods 9(12):1780. https://doi.org/10.3390/foods9121780

doi: 10.3390/foods9121780 pubmed: 33271757 pmcid: 7760545

Syrokou MK, Paramithiotis S, Drosinos EH, Bosnea L, Mataragas M (2022) A comparative genomic and safety assessment of six Lactiplantibacillus plantarum subsp. argentoratensis strains isolated from spontaneously fermented Greek wheat sourdoughs for potential biotechnological application. Int J Mol Sci 23(5):2487. https://doi.org/10.3390/ijms23052487

doi: 10.3390/ijms23052487 pubmed: 35269627 pmcid: 8910486

Hussein WE, Abdelhamid AG, Rocha-Mendoza D, García-Cano I, Yousef AE (2020) Assessment of safety and probiotic traits of Enterococcus durans OSY-EGY, isolated from Egyptian artisanal cheese, using comparative genomics and phenotypic analyses. Front Microbiol 11:608314. https://doi.org/10.3389/fmicb.2020.608314

doi: 10.3389/fmicb.2020.608314 pubmed: 33362752 pmcid: 7759505

Jiang S, Cai L, Lv L, Li L (2021) Pediococcus pentosaceus, a future additive or probiotic candidate. Microb Cell Fact 20(1):45. https://doi.org/10.1186/s12934-021-01537-y

doi: 10.1186/s12934-021-01537-y pubmed: 33593360 pmcid: 7885583

Pieniz S, Andreazza R, Anghinoni T et al (2014) Probiotic potential, antimicrobial and antioxidant activities of Enterococcus durans strain LAB18s. Food Control 37:251–256. https://doi.org/10.1016/j.foodcont.2013.09.055

doi: 10.1016/j.foodcont.2013.09.055

Escobar-Sánchez M, Carrasco-Navarro U, Juárez-Castelán C, Lozano-Aguirre Beltrán L, Pérez-Chabela ML, Ponce-Alquicira E (2023) Probiotic properties and proteomic analysis of Pediococcus pentosaceus 1101. Foods 12:46. https://doi.org/10.3390/foods12010046

doi: 10.3390/foods12010046

Bae WY, Lee YJ, Jung WH, Shin SL, Kim TR, Sohn M (2023) Draft genome sequence and probiotic functional property analysis of Lactobacillus gasseri LM1065 for food industry applications. Sci Rep 13(1):12212. https://doi.org/10.1038/s41598-023-39454-2

doi: 10.1038/s41598-023-39454-2 pubmed: 37500806 pmcid: 10374649

Darbandi A, Asadi A, Mahdizade Ari M et al (2022) Bacteriocins: properties and potential use as antimicrobials. J Clin Lab Anal 36(1):e24093. https://doi.org/10.1002/jcla.24093

doi: 10.1002/jcla.24093 pubmed: 34851542

Bosák J, Micenková L, Hrala M et al (2018) Colicin F

doi: 10.1038/s41598-018-30729-7 pubmed: 30115964 pmcid: 6095899

Khorshidian N, Khanniri E, Mohammadi M, Mortazavian AM, Yousefi M (2021) Antibacterial activity of pediocin and pediocin-producing bacteria against Listeria monocytogenes in meat products. Front Microbiol 12:709959. https://doi.org/10.3389/fmicb.2021.709959

doi: 10.3389/fmicb.2021.709959 pubmed: 34603234 pmcid: 8486284

Wang Y, You Y, Tian Y et al (2020) Pediococcus pentosaceus PP04 ameliorates high-fat diet-induced hyperlipidemia by regulating lipid metabolism in C57BL/6N mice. J Agric Food Chem 68(51):15154–15163. https://doi.org/10.1021/acs.jafc.0c05060

doi: 10.1021/acs.jafc.0c05060 pubmed: 33300795

Dubey V, Ghosh AR, Bishayee K, Khuda-Bukhsh AR (2016) Appraisal of the anti-cancer potential of probiotic Pediococcus pentosaceus GS4 against colon cancer: in vitro and in vivo approaches. Journal of Functional Foods 1(23):66–79

doi: 10.1016/j.jff.2016.02.032