Abstract
Pediococcus acidilactici is a reliable bacteriocin producer and a promising probiotic species with wide application in the food and health industry. However, the underlying genetic features of this species have not been analyzed. In this study, we performed a comprehensive comparative genomic analysis of 41 P. acidilactici strains from various ecological niches. The bacteriocin production of 41 strains were predicted and three kinds of bacteriocin encoding genes were identified in 11 P. acidilactici strains, namely pediocin PA-1, enterolysin A, and colicin-B. Moreover, whole-genome analysis showed a high genetic diversity within the population, mainly related to a large proportion of variable genomes, mobile elements, and hypothetical genes obtained through horizontal gene transfer. In addition, comparative genomics also facilitated the genetic explanation of the adaptation for host environment, which specify the protection mechanism against the invasion of foreign DNA (i.e. CRISPR/Cas locus), as well as carbohydrate fermentation. The 41 strains of P. acidilactici can metabolize a variety of carbon sources, which enhances the adaptability of this species and survival in different environments. This study evaluated the antibacterial ability, genome evolution, and ecological flexibility of P. acidilactici from the perspective of genetics and provides strong supporting evidence for its industrial development and application.
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Abu-Taraboush, H., Al-Dagal, M., and Al-Royli, M. 1998. Growth, viability, and proteolytic activity of Bifidobacteria in whole camel milk. J. Dairy Sci. 81, 354–361.
Altermann, E. 2012. Tracing lifestyle adaptation in prokaryotic genomes. Front. Microbiol. 3, 48.
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215, 403–410.
Anastasiadou, S., Papagianni, M., Filiousis, G., Ambrosiadis, I., and Koidis, P. 2008. Pediocin SA-1, an antimicrobial peptide from Pediococcus acidilactici NRRL B5627: Production conditions, purification and characterization. Bioresour. Technol. 99, 5384–5390.
Arber, W. 1991. Elements in microbial evolution. J. Mol. Evol. 33, 4–12.
Arboleya, S., Bottacini, F., O’Connell-Motherway, M., Ryan, C.A., Ross, R.P., Van Sinderen, D., and Stanton, C. 2018. Gene-trait matching across the Bifidobacterium longum pan-genome reveals considerable diversity in carbohydrate catabolism among human infant strains. BMC Genomics 19, 33.
Arndt, D., Grant, J.R., Marcu, A., Sajed, T., Pon, A., Liang, Y., and Wishart, D.S. 2016. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16–W21.
Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., Formsma, K., Gerdes, S., Glass, E.M., Kubal, M., et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9, 75.
Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A., and Horvath, P. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709–1712.
Bazinet, A.L. 2017. Pan-genome and phylogeny of Bacillus cereus sensu lato. BMC Evol. Biol. 17, 176.
Biswas, S., Ray, P., Johnson, M., and Ray, B. 1991. Influence of growth conditions on the production of a bacteriocin, pediocin AcH, by Pediococcus acidilactici H. Appl. Environ. Microbiol. 57, 1265–1267.
Burke, G.R. and Moran, N.A. 2011. Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol. Evol. 3, 195–208.
Cameron, A., Zaheer, R., Adator, E.H., Barbieri, R., Reuter, T., and McAllister, T.A. 2019. Bacteriocin occurrence and activity in Escherichia coli isolated from bovines and wastewater. Toxins 11, 475.
Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233–D238.
Carver, T.J., Rutherford, K.M., Berriman, M., Rajandream, M.A., Barrell, B.G., and Parkhill, J. 2005. ACT: the Artemis comparison tool. Bioinformatics 21, 3422–3423.
Chikindas, M.L., García-Garcerá, M.J., Driessen, A., Ledeboer, A.M., Nissen-Meyer, J., Nes, I.F., Abee, T., Konings, W.N., and Venema, G. 1993. Pediocin PA-1, a bacteriocin from Pediococcus acidilactici PAC1. 0, forms hydrophilic pores in the cytoplasmic membrane of target cells. Appl. Environ. Microbiol. 59, 3577–3584.
Cintas, L., Casaus, P., Fernández, M., and Hernández, P. 1998. Comparative antimicrobial activity of enterocin L50, pediocin PA-1, nisin A and lactocin S against spoilage and foodborne pathogenic bacteria. Food Microbiol. 15, 289–298.
Cintas, L.M., Rodriguez, J.M., Fernandez, M.F., Sletten, K., Nes, I.F., Hernandez, P.E., and Holo, H. 1995. Isolation and characterization of pediocin L50, a new bacteriocin from Pediococcus aci-dilactici with a broad inhibitory spectrum. Appl. Environ. Microbiol. 61, 2643–2648.
Contreras-Moreira, B. and Vinuesa, P. 2013. GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl. Environ. Microbiol. 79, 7696–7701.
Couvin, D., Bernheim, A., Toffano-Nioche, C., Touchon, M., Michalik, J., Néron, B., Rocha, E.P., Vergnaud, G., Gautheret, D., and Pourcel, C. 2018. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 46, W246–W251.
Dabour, N., Zihler, A., Kheadr, E., Lacroix, C., and Fliss, I. 2009. In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes. Int. J. Food Microbiol. 133, 225–233.
Drissi, F., Merhej, V., Angelakis, E., El Kaoutari, A., Carrière, F., Henrissat, B., and Raoult, D. 2014. Comparative genomics analysis of Lactobacillus species associated with weight gain or weight protection. Nutr. Diabetes 4, e109.
Elsinghorst, E.A. and Mortlock, R.P. 1988. D-Arabinose metabolism in Escherichia coli B: induction and cotransductional mapping of the l-fucose-d-arabinose pathway enzymes. J. Bacteriol. 170, 5423–5432.
Elsinghorst, E.A. and Mortlock, R.P. 1994. Molecular cloning of the Escherichia coli B L-fucose-D-arabinose gene cluster. J. Bacteriol. 176, 7223–7232.
Feng, J., Wang, L., Zhou, L., Yang, X., and Zhao, X. 2016. Using in vitro immunomodulatory properties of lactic acid bacteria for selection of probiotics against Salmonella infection in broiler chicks. PLoS ONE 11, e0147630.
Flint, H.J., Bayer, E.A., Rincon, M.T., Lamed, R., and White, B.A. 2008. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 6, 121–131.
Fu, J. and Qin, Q. 2012. Analysis of pan-genomic characteristics of 30 strains of E. coli. Genetic 34, 765–772.
Fuller, R. 1992. Probiotics: The scientific basis. Chapman & Hall, London, United Kingdom.
Goldin, B.R. and Gorbach, S.L. 1992. Probiotics for humans. In Fuller, R. (ed.) Probiotics. Springer, Dordrecht, Germany.
Henderson, J.T., Chopko, A.L., and Van Wassenaar, P.D. 1992. Purification and primary structure of pediocin PA-1 produced by Pediococcus acidilactici PAC-1.0. Arch. Biochem. Biophys. 295, 5–12.
Holzapfel, W.H., Franz, C.M.A.P., Ludwig, W., Back, W., and Dicks, L.M.T. 2006. The genera Pediococcus and Tetragenococcus. In Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., and Stackebrandt, E. (eds.), The Prokaryotes, pp. 229–266. Springer, New York, USA.
Horvath, P. and Barrangou, R. 2010. CRISPR/Cas, the immune system of bacteria and archaea. Science 327, 167–170.
Horvath, P., Coûté-Monvoisin, A.C., Romero, D.A., Boyaval, P., Fremaux, C., and Barrangou, R. 2009. Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int. J. Food Microbiol. 131, 62–70.
Jiang, J., Yang, B., Ross, R.P., Stanton, C., and Chen, W. 2020. Comparative genomics of Pediococcus pentosaceus isolated from different niches reveals genetic diversity in carbohydrate metabolism and immune system. Front. Microbiol. 11, 253.
Karp, P.D., Latendresse, M., Paley, S.M., Krummenacker, M., Ong, Q.D., Billington, R., Kothari, A., Weaver, D., Lee, T., Subhraveti, P., et al. 2016. Pathway tools version 19.0 update: software for pathway/genome informatics and systems biology. Brief. Bioinform. 17, 877–890.
Kelly, W.J., Cookson, A.L., Altermann, E., Lambie, S.C., Perry, R., Teh, K.H., Otter, D.E., Shapiro, N., Woyke, T., and Leahy, S.C. 2016. Genomic analysis of three Bifidobacterium species isolated from the calf gastrointestinal tract. Sci. Rep. 6, 30768.
Kolde, R. and Kolde, M.R. 2015. Package ‘pheatmap’. R package 1, 790.
Komora, N., Maciel, C., Pinto, C.A., Ferreira, V., Brandào, T.R., Saraiva, J.M., Castro, S.M., and Teixeira, P. 2020. Non-thermal approach to Listeria monocytogenes inactivation in milk: The combined effect of high pressure, pediocin PA-1 and bacteriophage P100. Food Microbiol. 86, 103315.
LeBlanc, D.J. and Mortlock, R.P. 1971. Metabolism of d-arabinose: a new pathway in Escherichia coli. J. Bacteriol. 106, 90–96.
Letunic, I. and Bork, P. 2016. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245.
Liu, Y., Harrison, P.M., Kunin, V., and Gerstein, M. 2004. Comprehensive analysis of pseudogenes in prokaryotes: widespread gene decay and failure of putative horizontally transferred genes. Genome Biol. 5, R64.
Lozano, J.C.N., Meyer, J.N., Sletten, K., Peláz, C., and Nes, I.F. 1992. Purification and amino acid sequence of a bacteriocin produced by Pediococcus acidilactici. Microbiology 138, 1985–1990.
Makarova, K.S., Wolf, Y.I., Alkhnbashi, O.S., Costa, F., Shah, S.A., Saunders, S.J., Barrangou, R., Brouns, S.J., Charpentier, E., Haft, D.H., et al. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13, 722–736.
Marri, P.R., Hao, W., and Golding, G.B. 2006. Gene gain and gene loss in Streptococcus: is it driven by habitat? Mol. Biol. Evol. 23, 2379–2391.
Mäyra-Mäkinen, A. and Bigret, M. 2004. Industrial use and production of lactic acid bacteria. In Salminen, S. and von Wright, A. (eds.), Lactic acid bacteria, Chapter 5. CRC Press, New York, USA.
Medini, D., Donati, C., Tettelin, H., Masignani, V., and Rappuoli, R. 2005. The microbial pan-genome. Curr. Opin. Genet. Dev. 15, 589–594.
Nieto-Lozano, J.C., Reguera-Useros, J.I., Peláez-Martínez, M.D.C., Sacristán-Pérez-Minayo, G., Gutiérrez-Fernández, A.J., and de la Torre, A.H. 2010. The effect of the pediocin PA-1 produced by Pediococcus acidilactici against Listeria monocytogenes and Clostridium perfringens in Spanish dry-fermented sausages and frankfurters. Food Control 21, 679–685.
Nissen-Meyer, J. and Nes, I.F. 1997. Ribosomally synthesized antimicrobial peptides: their function, structure, biogenesis, and mechanism of action. Arch. Microbiol. 167, 67–77.
O’Donnell, M.M., Forde, B.M., Neville, B., Ross, P.R., and O’Toole, P.W. 2011. Carbohydrate catabolic flexibility in the mammalian intestinal commensal Lactobacillus ruminis revealed by fermentation studies aligned to genome annotations. Microb. Cell Fact. 10, S12.
Olszewska, M. and Staniewski, B. 2012. Cell viability of Bifidobacterium lactis strain in long-term storage butter assessed with the plate count and fluorescence techniques. Czech J. Food Sci. 30, 421–428.
Parada, J.L., Caron, C.R., Medeiros, A.B.P., and Soccol, C.R. 2007. Bacteriocins from lactic acid bacteria: purification, properties and use as biopreservatives. Braz. Arch. Biol. Technol. 50, 512–542.
Porto, M.C.W., Kuniyoshi, T.M., Azevedo, P.O.S., Vitolo, M., and Oliveira, R.P.S. 2017. Pediococcus spp.: an important genus of lactic acid bacteria and pediocin producers. Biotechnol. Adv. 35, 361–374.
Rohman, A., Dijkstra, B.W., and Puspaningsih, N.N.T. 2019. β-Xylosidases: structural diversity, catalytic mechanism, and inhibition by monosaccharides. Int. J. Mol. Sci. 20, 5524.
Semjonovs, P. and Zikmanis, P. 2008. Evaluation of novel lactose-positive and exopolysaccharide-producing strain of Pediococcus pentosaceus for fermented foods. Eur. Food Res. Technol. 227, 851–856.
Shah, A.A., Yuan, X., Khan, R.U., and Shao, T. 2018. Effect of lactic acid bacteria-treated King grass silage on the performance traits and serum metabolites in New Zealand white rabbits (Oryctolagus cuniculus). J. Anim. Physiol. Anim. Nutr. 102, e902–e908.
Stiles, M.E. and Holzapfel, W.H. 1997. Lactic acid bacteria of foods and their current taxonomy. Int. J. Food Microbiol. 36, 1–29.
Tamura, K., Dudley, J., Nei, M., and Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.
Tarailo-Graovac, M. and Chen, N. 2004. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics 25, 4.10.1–4.110.14.
Tatusov, R.L., Galperin, M.Y., Natale, D.A., and Koonin, E.V. 2000. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33–36.
Tettelin, H., Riley, D., Cattuto, C., and Medini, D. 2008. Comparative genomics: the bacterial pan-genome. Curr. Opin. Microbiol. 11, 472–477.
Ueda, T., Tategaki, A., Hamada, K., Kishida, H., Nakagawa, K., Hosoe, K., Morikawa, H., and Nakagawa, K. 2018. Effects of Pediococcus acidilactici R037 on serum triglyceride levels in mice and rats after oral administration. J. Nutr. Sci. Vitaminol. 64, 41–47.
van Heel, A.J., de Jong, A., Song, C., Viel, J.H., Kok, J., and Kuipers, O.P.J.N.a.r. 2018. BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res. 46, W278–W281.
Waack, S., Keller, O., Asper, R., Brodag, T., Damm, C., Fricke, W.F., Surovcik, K., Meinicke, P., and Merkl, R. 2006. Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models. BMC Bioinformatics 7, 142.
Yang, X., Shi, P., Huang, H., Luo, H., Wang, Y., Zhang, W., and Yao, B. 2014. Two xylose-tolerant GH43 bifunctional β-xylosidase/α-arabinosidases and one GH11 xylanase from Humicola insolens and their synergy in the degradation of xylan. Food Chem. 148, 381–387.
Acknowledgements
We thank all members of the Guangdong Provincial Key Laboratory of core colletion of corp genetic resources research and application (NO.2011A091000047). This work was supported by the projects subsidized by special funds for science technology innovation and industrial development of Shenzhen Dapeng New District (Grand No. KJYF-202001-10).
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Li, Z., Song, Q., Wang, M. et al. Comparative genomics analysis of Pediococcus acidilactici species. J Microbiol. 59, 573–583 (2021). https://doi.org/10.1007/s12275-021-0618-6
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DOI: https://doi.org/10.1007/s12275-021-0618-6