1887

Abstract

The genera , , , and , which formed the family , have recently been merged within the family . Using genome sequences for 47 of the 52 named species from these genera, we report here comprehensive phylogenomic and comparative analyses on protein sequences from these species using multiple approaches. In a phylogenomic tree based on concatenated sequences of 498 core proteins from these five genera, and in a 16S rRNA gene tree, members of the genera , and formed distinct strongly supported clades. In contrast, species grouped into two distinct unrelated clades designated as the ‘ main clade’ and ‘ clade 2’. The presence of these clades is also seen in a matrix of pairwise average amino acid identity based on core protein sequences. In parallel, comparative genomic studies on protein sequences from genomes have identified 46 conserved signature indels (CSIs) in diverse proteins that are unique characteristics of the different observed species clades. Of these identified CSIs, five, five and 13 CSIs are uniquely present in members of the genera , and , respectively. We also report here six and five CSIs that are exclusively present in the species from the main clade and clade 2, respectively, providing independent evidence supporting their distinctness from each other. The remaining 12 identified CSIs are commonly shared by some or all of the species from the genera , and , clarifying their interrelationships. The identified CSIs provide novel and reliable means for the identification/circumscription of members of the genera , and as well as the two species clades in molecular terms. Based on the strong phylogenetic and molecular evidence presented here, we propose that the genus be limited to only the species from the a main clade, whereas the species forming clade 2 should be transferred to a new genus gen. nov.

Funding
This study was supported by the:
  • Natural Sciences and Engineering Research Council of Canada (Award RGPIN-2019-06397)
    • Principle Award Recipient: RadheyS. Gupta
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005284
2022-03-23
2022-07-06
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/72/3/ijsem005284.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.005284&mimeType=html&fmt=ahah

References

  1. Bello S, Rudra B, Gupta RS. Phylogenomic and comparative genomic analyses of Leuconostocaceae species: identification of molecular signatures specific for the genera Leuconostoc, Fructobacillus and Oenococcus and proposal for a novel genus Periweissella gen. nov. Figshare 2022. DOI: 10.6084/M9.FIGSHARE.18866273.V1
    [Google Scholar]
  2. Schleifer K-H. Family V. Leuconostocaceae fam. nov. In Jones D, Krieg NR, Ludwig W, Rainey FA. eds Bergey’s Manual of Systematic Bacteriology (The Firmicutes) New York: Springer; 2009
    [Google Scholar]
  3. Nieminen TT, Säde E, Endo A, Johansson P, Björkroth J et al. The family Leuconostocaceae. In Rosenberg E, DeLong EF, Lorey S. eds The Prokaryotes: Firmicutes and Tenericutes Springer-Verlag; 2014
    [Google Scholar]
  4. Holzapfel WH, Bjorkroth JA, Dicks LMT. Genus I. Leuconostoc van Tiegehem 1878, 198AL emend. mut. char. (Hucker and Pederson 1930), 66AL. In De Vos P, Jones D, Krieg NR, Ludwig W, Rainey FA. eds Bergey’s Manual of Systematic Bacteriology (The Firmicutes) New York: Springer; 2009 pp 624–636
    [Google Scholar]
  5. Bjorkroth JA, Dicks LMT, Holzapfel WH. Genus III. Weissella Collins, Samelis, Metaxopoulos and Wallbanks 1994, 370VP (effective publication: Collins, Samelis, Metaxopoulos, and Wallbanks 1993, 597). In De Vos P, Jones D, Krieg NR, Ludwig W, Rainey FA. eds Bergey’s Manual of Systematic Bacteriology (The Firmicutes) New York: Springer; 2009 pp 643–649
    [Google Scholar]
  6. Mokoena MP. Lactic acid bacteria and their bacteriocins: classification, biosynthesis and applications against uropathogens: a mini-review. Molecules 2017; 22:E1255 [View Article] [PubMed]
    [Google Scholar]
  7. Praet J, Meeus I, Cnockaert M, Houf K, Smagghe G et al. Novel lactic acid bacteria isolated from the bumble bee gut: Convivina intestini gen. nov., sp. nov., Lactobacillus bombicola sp. nov., and Weissella bombi sp. nov. Antonie van Leeuwenhoek 2015; 107:1337–1349 [View Article]
    [Google Scholar]
  8. Endo A, Okada S. Reclassification of the genus Leuconostoc and proposals of Fructobacillus fructosus gen. nov., comb. nov., Fructobacillus durionis comb. nov., Fructobacillus ficulneus comb. nov. and Fructobacillus pseudoficulneus comb. nov. Int J Syst Evol Microbiol 2008; 58:2195–2205 [View Article]
    [Google Scholar]
  9. Van Tieghem P. Sur la gomme de sucrerie (Leuconostoc mesenteroides). Annales des Sciences Naturelles Botanique 1878; 7:180–203 [View Article]
    [Google Scholar]
  10. Sneath PHA, McGowan V, Skerman VBD. Approved lists of bacterial names. Int J Syst Bacteriol 1980; 30:225–420 [View Article]
    [Google Scholar]
  11. Dicks LM, Dellaglio F, Collins MD. Proposal to reclassify Leuconostoc oenos as Oenococcus oeni [corrig.] gen. nov., comb. nov. Int J Syst Bacteriol 1995; 45:395–397 [View Article]
    [Google Scholar]
  12. Collins MD, Samelis J, Metaxopoulos J, Wallbanks S. Taxonomic studies on some leuconostoc-like organisms from fermented sausages: description of a new genus Weissella for the Leuconostoc paramesenteroides group of species. J Appl Bacteriol 1993; 75:595–603 [View Article] [PubMed]
    [Google Scholar]
  13. Zheng J, Wittouck S, Salvetti E, Franz CMAP, 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]
  14. Martinez-Murcia AJ, Collins MD. A phylogenetic analysis of the genus Leuconostoc based on reverse transcriptase sequencing of 16 S rRNA. FEMS Microbiol Lett 1990; 58:73–83 [View Article] [PubMed]
    [Google Scholar]
  15. Endo A, Maeno S, Tanizawa Y, Kneifel W, Arita M et al. Fructophilic lactic acid bacteria, a unique group of fructose-fermenting microbes. Appl Environ Microbiol 2018; 84:19 [View Article] [PubMed]
    [Google Scholar]
  16. Endo A, Tanizawa Y, Tanaka N, Maeno S, Kumar H et al. Comparative genomics of Fructobacillus spp. and Leuconostoc spp. reveals niche-specific evolution of Fructobacillus spp. BMC Genomics 2015; 16:1117 [View Article] [PubMed]
    [Google Scholar]
  17. 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; 84:17 [View Article] [PubMed]
    [Google Scholar]
  18. 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]
  19. Duar RM, Lin XB, Zheng J, Martino ME, Grenier T et al. Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Microbiol Rev 2017; 41:S27–S48 [View Article] [PubMed]
    [Google Scholar]
  20. Zheng J, Ruan L, Sun M, Gänzle M. A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology. Appl Environ Microbiol 2015; 81:7233–7243 [View Article] [PubMed]
    [Google Scholar]
  21. Chelo IM, Zé-Zé L, Tenreiro R. Congruence of evolutionary relationships inside the Leuconostoc-Oenococcus-Weissella clade assessed by phylogenetic analysis of the 16S rRNA gene, dnaA, gyrB, rpoC and dnaK. Int J Syst Evol Microbiol 2007; 57:276–286 [View Article] [PubMed]
    [Google Scholar]
  22. Endo A, Irisawa T, Futagawa-Endo Y, Sonomoto K, Itoh K et al. Fructobacillus tropaeoli sp. nov., a fructophilic lactic acid bacterium isolated from a flower. Int J Syst Evol Microbiol 2011; 61:898–902 [View Article] [PubMed]
    [Google Scholar]
  23. Nel S, Davis SB, Endo A, Dicks LMT. Phylogenetic analysis of Leuconostoc and Lactobacillus species isolated from sugarcane processing streams. Microbiologyopen 2020; 9:e1065 [View Article] [PubMed]
    [Google Scholar]
  24. Padonou SW, Schillinger U, Nielsen DS, Franz CMAP, Hansen M et al. Weissella beninensis sp. nov., a motile lactic acid bacterium from submerged cassava fermentations, and emended description of the genus Weissella. Int J Syst Evol Microbiol 2010; 60:2193–2198 [View Article] [PubMed]
    [Google Scholar]
  25. De Bruyne K, Camu N, De Vuyst L, Vandamme P. Weissella fabaria sp. nov., from a Ghanaian cocoa fermentation. Int J Syst Evol Microbiol 2010; 60:1999–2005 [View Article] [PubMed]
    [Google Scholar]
  26. Snauwaert I, Papalexandratou Z, De Vuyst L, Vandamme P. Characterization of strains of Weissella fabalis sp. nov. and Fructobacillus tropaeoli from spontaneous cocoa bean fermentations. Int J Syst Evol Microbiol 2013; 63:1709–1716 [View Article] [PubMed]
    [Google Scholar]
  27. Heo J, Hamada M, Cho H, Weon H-Y, Kim J-S et al. Weissella cryptocerci sp. nov., isolated from gut of the insect Cryptocercus kyebangensis. Int J Syst Evol Microbiol 2019; 69:2801–2806 [View Article]
    [Google Scholar]
  28. Li YQ, Tian WL, Gu CT. Weissella sagaensis sp. nov., isolated from traditional Chinese yogurt. Int J Syst Evol Microbiol 2020; 70:2485–2492 [View Article] [PubMed]
    [Google Scholar]
  29. Hyun D-W, Lee J-Y, Sung H, Kim PS, Jeong Y-S et al. Brevilactibacter coleopterorum sp. nov., isolated from the intestine of the dark diving beetle Hydrophilus acuminatus, and Weissella coleopterorum sp. nov., isolated from the intestine of the diving beetle Cybister lewisianus. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
    [Google Scholar]
  30. Oh SJ, Shin N-R, Hyun D-W, Kim PS, Kim JY et al. Weissella diestrammenae sp. nov., isolated from the gut of a camel cricket (Diestrammena coreana). Int J Syst Evol Microbiol 2013; 63:2951–2956 [View Article] [PubMed]
    [Google Scholar]
  31. Parte AC. LPSN - the list of prokaryotic names with standing in nomenclature. Int J Syst Evol Microbiol 2018; 68:1825–1829
    [Google Scholar]
  32. Mukherjee S, Seshadri R, Varghese NJ, Eloe-Fadrosh EA, Meier-Kolthoff JP et al. 1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life. Nat Biotechnol 2017; 35:676–683 [View Article] [PubMed]
    [Google Scholar]
  33. Whitman WB, Woyke T, Klenk H-P, Zhou Y, Lilburn TG et al. Genomic encyclopedia of bacterial and archaeal type strains, phase III: the genomes of soil and plant-associated and newly described type strains. Stand Genomic Sci 2015; 10:26 [View Article] [PubMed]
    [Google Scholar]
  34. Wu L, McCluskey K, Desmeth P, Liu S, Hideaki S et al. The global catalogue of microorganisms 10K type strain sequencing project: closing the genomic gaps for the validly published prokaryotic and fungi species. Gigascience 2018; 7: [View Article] [PubMed]
    [Google Scholar]
  35. Konstantinidis KT, Tiedje JM. Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 2007; 10:504–509 [View Article] [PubMed]
    [Google Scholar]
  36. Gupta RS. Protein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 1998; 62:1435–1491 [View Article] [PubMed]
    [Google Scholar]
  37. Gupta RS. Identification of conserved indels that are useful for classification and evolutionary studies. In Goodfellow M, Sutcliffe IC, Chun J. eds Bacterial Taxonomy, Methods in Microbiology vol 41 London: Elsevier; 2014 pp 153–182
    [Google Scholar]
  38. Gupta RS. Impact of genomics on clarifying the evolutionary relationships amongst mycobacteria: identification of molecular signatures specific for the tuberculosis-complex of bacteria with potential applications for novel diagnostics and therapeutics. High Throughput 2018; 7:E31 [View Article] [PubMed]
    [Google Scholar]
  39. Gupta RS. Impact of genomics on the understanding of microbial evolution and classification: the importance of Darwin’s views on classification. FEMS Microbiol Rev 2016; 40:520–553 [View Article] [PubMed]
    [Google Scholar]
  40. Gupta RS. Microbial taxonomy: how and why name changes occur and their significance for (clinical) microbiology. Clin Chem 2021; 68:134–137 [View Article] [PubMed]
    [Google Scholar]
  41. Patel S, Gupta RS. A phylogenomic and comparative genomic framework for resolving the polyphyly of the genus Bacillus: Proposal for six new genera of Bacillus species, Peribacillus gen. nov., Cytobacillus gen. nov., Mesobacillus gen. nov., Neobacillus gen. nov., Metabacillus gen. nov. and Alkalihalobacillus gen. nov. Int J Syst Evol Microbiol 2020; 70:406–438 [View Article]
    [Google Scholar]
  42. Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the “Enterobacteriales”: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016; 66:5575–5599 [View Article]
    [Google Scholar]
  43. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012; 28:3150–3152 [View Article] [PubMed]
    [Google Scholar]
  44. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article] [PubMed]
    [Google Scholar]
  45. Sonnhammer EL, Eddy SR, Birney E, Bateman A, Durbin R. Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res 1998; 26:320–322 [View Article] [PubMed]
    [Google Scholar]
  46. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article] [PubMed]
    [Google Scholar]
  47. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  48. Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001; 18:691–699 [View Article] [PubMed]
    [Google Scholar]
  49. Le SQ, Lartillot N, Gascuel O. Phylogenetic mixture models for proteins. Philos Trans R Soc Lond B Biol Sci 2008; 363:3965–3976 [View Article] [PubMed]
    [Google Scholar]
  50. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  51. Thompson CC, Chimetto L, Edwards RA, Swings J, Stackebrandt E et al. Microbial genomic taxonomy. BMC Genomics 2013; 14:913 [View Article] [PubMed]
    [Google Scholar]
  52. Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res 2014; 42:D643–8 [View Article] [PubMed]
    [Google Scholar]
  53. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526 [View Article] [PubMed]
    [Google Scholar]
  54. Naushad HS, Lee B, Gupta RS. Conserved signature indels and signature proteins as novel tools for understanding microbial phylogeny and systematics: identification of molecular signatures that are specific for the phytopathogenic genera Dickeya, Pectobacterium and Brenneria. Int J Syst Evol Microbiol 2014; 64:366–383 [View Article] [PubMed]
    [Google Scholar]
  55. Bello S, Rudra B, Gupta RS. Supplemental data: phylogenomic and comparative genomic analyses on Leuconostocaceae species: identification of molecular signatures specific for the genera Leuconostoc, Fructobacillus and Oenococcus and proposal for a novel genus Periweissella gen. nov. Int J Syst Evol Microbiol 20221–108 [View Article]
    [Google Scholar]
  56. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article] [PubMed]
    [Google Scholar]
  57. Dobritsa AP, Samadpour M. Reclassification of Burkholderia insecticola as Caballeronia insecticola comb. nov. and reliability of conserved signature indels as molecular synapomorphies. Int J Syst Evol Microbiol 2019; 69:2057–2063 [View Article] [PubMed]
    [Google Scholar]
  58. Parker C, Tindall BJ, Garrity GM. International Code of Nomenclature of Prokaryotes. Int J Syst Evol Microbiol 2019; 69:S1–S111 [View Article] [PubMed]
    [Google Scholar]
  59. Chelo IM, Zé-Zé L, Tenreiro R. Genome diversity in the genera Fructobacillus, Leuconostoc and Weissella determined by physical and genetic mapping. Microbiology (Reading) 2010; 156:420–430 [View Article] [PubMed]
    [Google Scholar]
  60. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2019btz848 [View Article] [PubMed]
    [Google Scholar]
  61. Collins MD, Samelis J, Metaxopoulous J, Wallbanks S. Validation of the publication of new names and new combinations previously effectively published outside the IJSB: List No. 49. Int J Syst Bacteriol 1994; 44:370–371 [View Article]
    [Google Scholar]
  62. Rokas A, Holland PW. Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 2000; 15:454–459 [View Article] [PubMed]
    [Google Scholar]
  63. Barbour AG, Adeolu M, Gupta RS. Division of the genus Borrelia into two genera (corresponding to Lyme disease and relapsing fever groups) reflects their genetic and phenotypic distinctiveness and will lead to a better understanding of these two groups of microbes (Margos et al. (2016) There is inadequate evidence to support the division of the genus Borrelia. Int J Syst Evol Microbiol 2017; 67:2058–2067 [View Article]
    [Google Scholar]
  64. De Bruyne K, Camu N, Lefebvre K, De Vuyst L, Vandamme P. Weissella ghanensis sp. nov., isolated from a Ghanaian cocoa fermentation. Int J Syst Evol Microbiol 2008; 58:2721–2725 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005284
Loading
/content/journal/ijsem/10.1099/ijsem.0.005284
Loading

Data & Media loading...

Supplements

Loading data from figshare Loading data from figshare

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error