1887

Abstract

The genus (formerly ) contains multiple species considered to be adapted to vertebrates, yet their genomic diversity has not been explored. In this study, we performed comparative genomic analysis of (22 species; 332 genomes) isolated from different niches, further focusing on human strains (11 species; 74 genomes) and their adaptation features to specific body sites. Phylogenomic analysis of showed misidentification of some strains deposited in public databases and existence of putative novel species. The pangenome analysis revealed a remarkable genomic diversity (only 1.3 % of gene clusters are shared), and we did not observe a strong association of the accessory genome with different niches. The pangenome of and was open, suggesting that acquisition of genes is still occurring. Although most were predicted as antibiotic susceptible (83%), acquired antibiotic-resistance genes were common in from food-producing animals. Genes related to lactic acid isoform production (>95 %) and putative bacteriocins (70.2%) were identified in most strains, while prophages (55.4%) and CRISPR-Cas systems (32.0%) were less prevalent. Among strains from human sources, several metabolic pathways were predicted as conserved and completed. Their accessory genome was highly variable and did not cluster according to different human body sites, with some exceptions (urogenital , , and or gastrointestinal ). Moreover, we identified 12 Kyoto Encyclopedia of Genes and Genomes (KEGG) orthologues that were significantly enriched in strains from particular body sites. We concluded that evolution of the highly diverse is complex and not always related to niche or human body site origin.

Funding
This study was supported by the:
  • Unidade de Ciências Biomoleculares Aplicada (Award UIDP/QUI/04378/2020)
    • Principle Award Recipient: TeresaMaria Pinto Gonçalves Ribeiro
  • Fundação para a Ciência e a Tecnologia (Award DL57/2016/CP1346/CT0034)
    • Principle Award Recipient: FilipaGrosso
  • Fundação para a Ciência e a Tecnologia (Award SFRH/BD/132497/2017)
    • Principle Award Recipient: MagdalenaKsiezarek
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2022-07-15
2024-04-29
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References

  1. Ksiezarek M, Grosso F, Ribeiro TG, Peixe L. Genomic diversity of genus Limosilactobacillus Figshare 2022 [View Article]
    [Google Scholar]
  2. Salvetti E, Harris HMB, Felis GE, O’Toole PW. Comparative genomics of the genus Lactobacillus reveals robust phylogroups that provide the basis for reclassification. Appl Environ Microbiol 2018; 84:e00993-18 [View Article] [PubMed]
    [Google Scholar]
  3. Zheng J, Wittouck S, Salvetti E, Franz C, Harris HMB et al. A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 2020; 70:2782–2858 [View Article] [PubMed]
    [Google Scholar]
  4. Ksiezarek M, Ribeiro TG, Rocha J, Grosso F, Perovic SU et al. Limosilactobacillus urinaemulieris sp. nov. and limosilactobacillus portuensis sp. nov. isolated from urine of healthy women. Int J Syst Evol Microbiol 2021; 71:004726
    [Google Scholar]
  5. Li F, Cheng CC, Zheng J, Liu J, Quevedo RM et al. Limosilactobacillus balticus sp. nov., Limosilactobacillus agrestis sp. nov., Limosilactobacillus albertensis sp. nov., Limosilactobacillus rudii sp. nov. and Limosilactobacillus fastidiosus sp. nov., five novel Limosilactobacillus species isolated from the vertebrate gastrointestinal tract, and proposal of six subspecies of Limosilactobacillus reuteri adapted to the gastrointestinal tract of specific vertebrate hosts. Int J Syst Evol Microbiol 2021; 71:004644 [View Article]
    [Google Scholar]
  6. Naghmouchi K, Belguesmia Y, Bendali F, Spano G, Seal BS et al. Lactobacillus fermentum: a bacterial species with potential for food preservation and biomedical applications. Crit Rev Food Sci Nutr 2020; 60:3387–3399 [View Article] [PubMed]
    [Google Scholar]
  7. Mu Q, Tavella VJ, Luo XM. Role of Lactobacillus reuteri in human health and diseases. Front Microbiol 2018; 9:757 [View Article] [PubMed]
    [Google Scholar]
  8. Pasolli E, De Filippis F, Mauriello IE, Cumbo F, Walsh AM et al. Large-scale genome-wide analysis links lactic acid bacteria from food with the gut microbiome. Nat Commun 2020; 11:2610 [View Article] [PubMed]
    [Google Scholar]
  9. Ksiezarek M, Ugarcina-Perovic S, Rocha J, Grosso F, Peixe L. Long-term stability of the urogenital microbiota of asymptomatic European women. BMC Microbiol 2021; 21:64 [View Article] [PubMed]
    [Google Scholar]
  10. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  11. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  12. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 2016; 8:12–24 [View Article]
    [Google Scholar]
  13. Ramasamy D, Mishra AK, Lagier J-C, Padhmanabhan R, Rossi M et al. A polyphasic strategy incorporating genomic data for the taxonomic description of novel bacterial species. Int J Syst Evol Microbiol 2014; 64:384–391 [View Article] [PubMed]
    [Google Scholar]
  14. R Core TeamR: a Language and Environment for Statistical Computing Vienna: R Foundation for Statistical Computing; 2018 https://www.R-project.org/
  15. Eren AM, Kiefl E, Shaiber A, Veseli I, Miller SE et al. Community-led, integrated, reproducible multi-omics with anvi’o. Nat Microbiol 2021; 6:3–6 [View Article] [PubMed]
    [Google Scholar]
  16. Lee MD. GToTree: a user-friendly workflow for phylogenomics. Bioinformatics 2019; 35:4162–4164 [View Article] [PubMed]
    [Google Scholar]
  17. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 2009; 26:1641–1650 [View Article] [PubMed]
    [Google Scholar]
  18. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
    [Google Scholar]
  19. Inkscape Project Inkscape; 2020 https://inkscape.org
  20. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
    [Google Scholar]
  21. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2012; 40:D109–D114 [View Article] [PubMed]
    [Google Scholar]
  22. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  23. van Dongen S, Abreu-Goodger C. Using MCL to extract clusters from networks. Methods Mol Biol 2012; 804:281–295 [View Article] [PubMed]
    [Google Scholar]
  24. Wickham H. ggplot2: Elegant Graphics for Data Analysis New York: Springer-Verlag; 2016 https://ggplot2.tidyverse.org
  25. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  26. Chen H, Boutros PC. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics 2011; 12:35 [View Article] [PubMed]
    [Google Scholar]
  27. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013; 8:e61217 [View Article] [PubMed]
    [Google Scholar]
  28. Shaiber A, Willis AD, Delmont TO, Roux S, Chen L-X et al. Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome. Genome Biol 2020; 21:292 [View Article] [PubMed]
    [Google Scholar]
  29. van Heel AJ, de Jong A, Song C, Viel JH, Kok J et al. BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res 2018; 46:W278–W281 [View Article] [PubMed]
    [Google Scholar]
  30. Russel J, Pinilla-Redondo R, Mayo-Muñoz D, Shah SA, Sørensen SJ. CRISPRCasTyper: automated identification, annotation, and classification of CRISPR-Cas loci. CRISPR J 2020; 3:462–469 [View Article] [PubMed]
    [Google Scholar]
  31. Akhter S, Aziz RK, Edwards RA. PhiSpy: a novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies. Nucleic Acids Res 2012; 40:e126 [View Article] [PubMed]
    [Google Scholar]
  32. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  33. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
    [Google Scholar]
  34. Cárdenas N, Laiño JE, Delgado S, Jiménez E, Juárez del Valle M et al. Relationships between the genome and some phenotypical properties of Lactobacillus fermentum CECT 5716, a probiotic strain isolated from human milk. Appl Microbiol Biotechnol 2015; 99:4343–4353 [View Article] [PubMed]
    [Google Scholar]
  35. Sun Z, Harris HMB, McCann A, Guo C, Argimón S et al. Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera. Nat Commun 2015; 6:8322 [View Article] [PubMed]
    [Google Scholar]
  36. Kant R, Blom J, Palva A, Siezen RJ, de Vos WM. Comparative genomics of Lactobacillus. Microb Biotechnol 2011; 4:323–332 [View Article] [PubMed]
    [Google Scholar]
  37. Yu J, Zhao J, Song Y, Zhang J, Yu Z et al. Comparative genomics of the herbivore gut symbiont Lactobacillus reuteri reveals genetic diversity and lifestyle adaptation. Front Microbiol 2018; 9:1151 [View Article] [PubMed]
    [Google Scholar]
  38. Illeghems K, De Vuyst L, Weckx S. Comparative genome analysis of the candidate functional starter culture strains Lactobacillus fermentum 222 and Lactobacillus plantarum 80 for controlled cocoa bean fermentation processes. BMC Genomics 2015; 16:766 [View Article] [PubMed]
    [Google Scholar]
  39. Brockhurst MA, Harrison E, Hall JPJ, Richards T, McNally A et al. The ecology and evolution of pangenomes. Curr Biol 2019; 29:R1094–R1103 [View Article] [PubMed]
    [Google Scholar]
  40. Chen L, Gu Q, Li P, Chen S, Li Y. Genomic analysis of Lactobacillus reuteri WHH1689 reveals its probiotic properties and stress resistance. Food Sci Nutr 2019; 7:844–857 [View Article] [PubMed]
    [Google Scholar]
  41. Xu S, Cheng J, Meng X, Xu Y, Mu Y. Complete genome and comparative genome analysis of Lactobacillus reuteri YSJL-12, a potential probiotics strain isolated from healthy sow fresh feces. Evol Bioinform Online 2020; 16:1176934320942192 [View Article] [PubMed]
    [Google Scholar]
  42. Yoo D, Bagon BB, Valeriano VDV, Oh JK, Kim H et al. Complete genome analysis of Lactobacillus fermentum SK152 from kimchi reveals genes associated with its antimicrobial activity. FEMS Microbiol Lett 2017; 364:fnx185 [View Article] [PubMed]
    [Google Scholar]
  43. Brandt K, Nethery MA, O’Flaherty S, Barrangou R. Genomic characterization of Lactobacillus fermentum DSM 20052. BMC Genomics 2020; 21:328 [View Article] [PubMed]
    [Google Scholar]
  44. Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW et al. The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome 2014; 2:4 [View Article] [PubMed]
    [Google Scholar]
  45. Das Purkayastha S, Bhattacharya MK, Prasad HK, Upadhyaya H, Lala SD et al. Contrasting diversity of vaginal lactobacilli among the females of Northeast India. BMC Microbiol 2019; 19:198 [View Article] [PubMed]
    [Google Scholar]
  46. Soto A, Martín V, Jiménez E, Mader I, Rodríguez JM et al. Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors. J Pediatr Gastroenterol Nutr 2014; 59:78–88 [View Article] [PubMed]
    [Google Scholar]
  47. Belstrøm D, Constancias F, Liu Y, Yang L, Drautz-Moses DI et al. Metagenomic and metatranscriptomic analysis of saliva reveals disease-associated microbiota in patients with periodontitis and dental caries. NPJ Biofilms Microbiomes 2017; 3:23 [View Article] [PubMed]
    [Google Scholar]
  48. Million M, Maraninchi M, Henry M, Armougom F, Richet H et al. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int J Obes 2012; 36:817–825 [View Article] [PubMed]
    [Google Scholar]
  49. Inglin RC, Meile L, Stevens MJA. Clustering of pan- and core-genome of Lactobacillus provides novel evolutionary insights for differentiation. BMC Genomics 2018; 19:284 [View Article] [PubMed]
    [Google Scholar]
  50. Mendes-Soares H, Suzuki H, Hickey RJ, Forney LJ. Comparative functional genomics of Lactobacillus spp. reveals possible mechanisms for specialization of vaginal lactobacilli to their environment. J Bacteriol 2014; 196:1458–1470 [View Article] [PubMed]
    [Google Scholar]
  51. Valeriano VDV, Oh JK, Bagon BB, Kim H, Kang D-K. Comparative genomic analysis of Lactobacillus mucosae LM1 identifies potential niche-specific genes and pathways for gastrointestinal adaptation. Genomics 2019; 111:24–33 [View Article] [PubMed]
    [Google Scholar]
  52. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B et al. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 2006; 103:15611–15616 [View Article] [PubMed]
    [Google Scholar]
  53. Hernández-Montes G, Díaz-Mejía JJ, Pérez-Rueda E, Segovia L. The hidden universal distribution of amino acid biosynthetic networks: a genomic perspective on their origins and evolution. Genome Biol 2008; 9:R95 [View Article] [PubMed]
    [Google Scholar]
  54. Peterson CT, Rodionov DA, Osterman AL, Peterson SN. B vitamins and their role in immune regulation and cancer. Nutrients 2020; 12:E3380 [View Article] [PubMed]
    [Google Scholar]
  55. Yoshii K, Hosomi K, Sawane K, Kunisawa J. Metabolism of dietary and microbial vitamin B family in the regulation of host immunity. Front Nutr 2019; 6:48 [View Article] [PubMed]
    [Google Scholar]
  56. Verce M, De Vuyst L, Weckx S. Comparative genomics of Lactobacillus fermentum suggests a free-living lifestyle of this lactic acid bacterial species. Food Microbiol 2020; 89:103448 [View Article] [PubMed]
    [Google Scholar]
  57. Oh PL, Benson AK, Peterson DA, Patil PB, Moriyama EN et al. Diversification of the gut symbiont Lactobacillus reuteri as a result of host-driven evolution. ISME J 2010; 4:377–387 [View Article] [PubMed]
    [Google Scholar]
  58. Frese SA, Benson AK, Tannock GW, Loach DM, Kim J et al. The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet 2011; 7:e1001314 [View Article] [PubMed]
    [Google Scholar]
  59. Bui TPN, Ritari J, Boeren S, de Waard P, Plugge CM et al. Production of butyrate from lysine and the Amadori product fructoselysine by a human gut commensal. Nat Commun 2015; 6:10062 [View Article] [PubMed]
    [Google Scholar]
  60. Pokharel S, Shrestha P, Adhikari B. Antimicrobial use in food animals and human health: time to implement “One Health” approach. Antimicrob Resist Infect Control 2020; 9:181 [View Article] [PubMed]
    [Google Scholar]
  61. Lazarus B, Paterson DL, Mollinger JL, Rogers BA. Do human extraintestinal Escherichia coli infections resistant to expanded-spectrum cephalosporins originate from food-producing animals? A systematic review. Clin Infect Dis 2015; 60:439–452 [View Article] [PubMed]
    [Google Scholar]
  62. Aarestrup FM. The livestock reservoir for antimicrobial resistance: a personal view on changing patterns of risks, effects of interventions and the way forward. Philos Trans R Soc Lond B Biol Sci 2015; 370:20140085 [View Article] [PubMed]
    [Google Scholar]
  63. Butiuc-Keul A, Farkas A, Carpa R, Iordache D. CRISPR-Cas system: the powerful modulator of accessory genomes in prokaryotes. Microb Physiol 2022; 32:2–17 [View Article] [PubMed]
    [Google Scholar]
  64. Chylinski K, Makarova KS, Charpentier E, Koonin EV. Classification and evolution of type II CRISPR-Cas systems. Nucleic Acids Res 2014; 42:6091–6105 [View Article] [PubMed]
    [Google Scholar]
  65. Shmakov SA, Sitnik V, Makarova KS, Wolf YI, Severinov KV et al. The CRISPR spacer space is dominated by sequences from species-specific mobilomes. mBio 2017; 8:e01397-17 [View Article] [PubMed]
    [Google Scholar]
  66. Yang L, Li W, Ujiroghene OJ, Yang Y, Lu J et al. Occurrence and diversity of CRISPR loci in Lactobacillus casei group. Front Microbiol 2020; 11:624 [View Article] [PubMed]
    [Google Scholar]
  67. de Jesus LCL, Drumond MM, Aburjaile FF, Sousa T de J, Coelho-Rocha ND et al. Probiogenomics of Lactobacillus delbrueckii subsp. lactis cidca 133: in silico, in vitro, and in vivo approaches. Microorganisms 2021; 9:829 [View Article]
    [Google Scholar]
  68. Khan H, Flint SH, Yu P-L. Determination of the mode of action of enterolysin A, produced by Enterococcus faecalis B9510. J Appl Microbiol 2013; 115:484–494 [View Article] [PubMed]
    [Google Scholar]
  69. Nilsen T, Nes IF, Holo H. Enterolysin A, A cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Appl Environ Microbiol 2003; 69:2975–2984 [View Article] [PubMed]
    [Google Scholar]
  70. Alvarez-Sieiro P, Montalbán-López M, Mu D, Kuipers OP. Bacteriocins of lactic acid bacteria: extending the family. Appl Microbiol Biotechnol 2016; 100:2939–2951 [View Article] [PubMed]
    [Google Scholar]
  71. Nilsen T, Swedek I, Lagenaur LA, Parks TP. Novel selective inhibition of Lactobacillus iners by Lactobacillus-derived bacteriocins. Appl Environ Microbiol 2020; 86:e01594-20 [View Article] [PubMed]
    [Google Scholar]
  72. Davidson BE, Kordias N, Dobos M, Hillier AJ. Genomic organization of lactic acid bacteria. Antonie Van Leeuwenhoek 1996; 70:161–183 [View Article] [PubMed]
    [Google Scholar]
  73. Mercanti DJ, Carminati D, Reinheimer JA, Quiberoni A. Widely distributed lysogeny in probiotic lactobacilli represents a potentially high risk for the fermentative dairy industry. Int J Food Microbiol 2011; 144:503–510 [View Article] [PubMed]
    [Google Scholar]
  74. Manrique P, Dills M, Young MJ. The human gut phage community and its implications for health and disease. Viruses 2017; 9:E141 [View Article] [PubMed]
    [Google Scholar]
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