1887

Abstract

Strain LMG 33000 was isolated from a gut sample. It shared the highest percentage 16S rRNA sequence identity, average amino acid identity, and amino acid identity of conserved genes with LMG 28291 (95.86 %, 69.9 and 76.2 %, respectively), and the highest percentage OrthoANIu value with DSM 20349 (71.4 %). Phylogenomic analyses by means of 107 or 120 conserved genes consistently revealed as nearest neighbour genus. The draft genome of strain LMG 33000 was 1.44 Mbp in size and had a DNA G+C content of 46.1 mol%. Genomic and physiological analyses revealed that strain LMG 33000 was a typical obligately fructophilic lactic acid bacterium that lacked the and genes and that did not produce ethanol during glucose or fructose metabolism. In contrast, species have the and genes in their genomes and produced ethanol from glucose and fructose metabolism, which is typical for heterofermentative lactic acid bacteria. Moreover, strain LMG 33000 exhibited catalase activity, an unusual characteristic among lactic acid bacteria, that is not shared with species. Given its position in the phylogenomic trees, and the difference in genomic percentage G+C content and in physiological and metabolic characteristics between strain LMG 33000 and species, we considered it most appropriate to classify strain LMG 33000 into a novel genus and species within the family for which we propose the name gen. nov., sp. nov., with LMG 33000 (=CECT 30958) as the type strain.

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2024-06-04
2024-06-17
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References

  1. 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:e01290-18 [View Article] [PubMed]
    [Google Scholar]
  2. 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] [PubMed]
    [Google Scholar]
  3. Gallus MK, Beer I, Ivleva NP, Ehrmann MA. Fructobacillus cardui sp. nov., isolated from a thistle (Carduus nutans) flower. Int J Syst Evol Microbiol 2022; 72: [View Article]
    [Google Scholar]
  4. Lin ST, Guu JR, Wang HM, Tamura T, Mori K et al. Fructobacillus papyriferae sp. nov., Fructobacillus papyrifericola sp. nov., Fructobacillus broussonetiae sp. nov. and Fructobacillus parabroussonetiae sp. nov., isolated from paper mulberry in Taiwan. Int J Syst Evolution Microbiol 2022; 72: [View Article]
    [Google Scholar]
  5. Endo A, Futagawa-Endo Y, Dicks LMT. Isolation and characterization of fructophilic lactic acid bacteria from fructose-rich niches. Syst Appl Microbiol 2009; 32:593–600 [View Article] [PubMed]
    [Google Scholar]
  6. Endo A, Futagawa-Endo Y, Sakamoto M, Kitahara M, Dicks LMT. Lactobacillus florum sp. nov., a fructophilic species isolated from flowers. Int J Syst Evol Microbiol 2010; 60:2478–2482 [View Article] [PubMed]
    [Google Scholar]
  7. Oliphant SA, Watson-Haigh NS, Sumby KM, Gardner J, Groom S et al. Apilactobacillus apisilvae sp. nov., Nicolia spurrieriana gen. nov. sp. nov., Bombilactobacillus folatiphilus sp. nov. and Bombilactobacillus thymidiniphilus sp. nov., four new lactic acid bacterial isolates from stingless bees Tetragonula carbonaria and Austroplebeia australis. Int J Syst Evol Microbiol 2022; 72: [View Article]
    [Google Scholar]
  8. Kouya T, Ishiyama Y, Ohashi S, Kumakubo R, Yamazaki T et al. Philodulcilactobacillus myokoensis gen. nov., sp. nov., a fructophilic, acidophilic, and agar-phobic lactic acid bacterium isolated from fermented vegetable extracts. PLoS One 2023; 18:e0286677 [View Article] [PubMed]
    [Google Scholar]
  9. Chen Y, Wang L-T, Lin S-T, Lee Y-S, Chang Y-C et al. Fructobacillus apis sp. nov., isolated from the gut of honeybee (Apis mellifera). Int J Syst Evol Microbiol 2022; 72: [View Article]
    [Google Scholar]
  10. Neveling DP, Endo A, Dicks LMT. Fructophilic Lactobacillus kunkeei and Lactobacillus brevis isolated from fresh flowers, bees and bee-hives. Curr Microbiol 2012; 65:507–515 [View Article] [PubMed]
    [Google Scholar]
  11. Oliphant SA, Watson-Haigh NS, Sumby KM, Gardner JM, Jiranek V. Fructilactobacillus cliffordii sp. nov., Fructilactobacillus hinvesii sp. nov., Fructilactobacillus myrtifloralis sp. nov., Fructilactobacillus carniphilus sp. nov. and Fructobacillus americanaquae sp. nov., five novel lactic acid bacteria isolated from insects or flowers of Kangaroo Island, South Australia. Int J Syst Evol Microbiol 2023; 73: [View Article]
    [Google Scholar]
  12. Praet J, Parmentier A, Schmid-Hempel R, Meeus I, Smagghe G et al. Large-scale cultivation of the bumblebee gut microbiota reveals an underestimated bacterial species diversity capable of pathogen inhibition. Environ Microbiol 2018; 20:214–227 [View Article] [PubMed]
    [Google Scholar]
  13. Hettiarachchi A, Cnockaert M, Joossens M, Laureys D, De Clippeleer J et al. Convivina is a specialised core gut symbiont of the invasive hornet Vespa velutina. Insect Mol Biol 2023; 32:510–527 [View Article] [PubMed]
    [Google Scholar]
  14. Engel P, Kwong WK, McFrederick Q, Anderson KE, Barribeau SM et al. The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions. mBio 2016; 7:e02164-15 [View Article] [PubMed]
    [Google Scholar]
  15. Rothman JA, Leger L, Graystock P, Russell K, McFrederick QS. The bumble bee microbiome increases survival of bees exposed to selenate toxicity. Environ Microbiol 2019; 21:3417–3429 [View Article] [PubMed]
    [Google Scholar]
  16. Voulgari-Kokota A, McFrederick QS, Steffan-Dewenter I, Keller A. Drivers, diversity, and functions of the solitary-bee microbiota. Trends Microbiol 2019; 27:1034–1044 [View Article] [PubMed]
    [Google Scholar]
  17. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:i884–i890 [View Article] [PubMed]
    [Google Scholar]
  18. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  19. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
    [Google Scholar]
  20. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
    [Google Scholar]
  21. Okonechnikov K, Conesa A, García-Alcalde F. Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 2016; 32:292–294 [View Article] [PubMed]
    [Google Scholar]
  22. 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]
  23. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  24. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  25. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
    [Google Scholar]
  26. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinform 2009; 10:421 [View Article] [PubMed]
    [Google Scholar]
  27. Ankenbrand MJ, Keller A. bcgTree: automatized phylogenetic tree building from bacterial core genomes. Genome 2016; 59:783–791 [View Article] [PubMed]
    [Google Scholar]
  28. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics 2022; 38:5315–5316 [View Article] [PubMed]
    [Google Scholar]
  29. Letunic I, Bork P. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 2021; 49:W293–W296 [View Article] [PubMed]
    [Google Scholar]
  30. Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 2019; 20:238 [View Article] [PubMed]
    [Google Scholar]
  31. Buchfink B, Reuter K, Drost HG. Sensitive protein alignments at tree-of-life scale using diamond. Nat Methods 2021; 18:366–368 [View Article] [PubMed]
    [Google Scholar]
  32. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: founctional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article] [PubMed]
    [Google Scholar]
  33. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article] [PubMed]
    [Google Scholar]
  34. Ruiz-Perez CA, Conrad RE, Konstantinidis KT. MicrobeAnnotator: a user-friendly, comprehensive functional annotation pipeline for microbial genomes. BMC Bioinform 2021; 22:11 [View Article] [PubMed]
    [Google Scholar]
  35. Zheng J, Ge Q, Yan Y, Zhang X, Huang L et al. dbCAN3: automated carbohydrate-active enzyme and substrate annotation. Nucleic Acids Res 2023; 51:W115–W121 [View Article] [PubMed]
    [Google Scholar]
  36. Hitch TCA, Riedel T, Oren A, Overmann J, Lawley TD et al. Automated analysis of genomic sequences facilitates high-throughput and comprehensive description of bacteria. ISME Commun 2021; 1:16 [View Article] [PubMed]
    [Google Scholar]
  37. Macfaddin JF. Biochemical Tests for Identification of Medical Bacteria, 3rd edn Baltimore: Williams and Wilkins; 2000
    [Google Scholar]
  38. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S et al. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 2011; 20:619–628 [View Article] [PubMed]
    [Google Scholar]
  39. Sarton-Lohéac G, Nunes da Silva CG, Mazel F, Baud G, de Bakker V et al. Deep divergence and genomic diversification of gut symbionts of neotropical stingless bees. mBio 2023; 14:e0353822 [View Article] [PubMed]
    [Google Scholar]
  40. Aarnikunnas J, Rönnholm K, Palva A. The mannitol dehydrogenase gene (mdh) from Leuconostoc mesenteroides is distinct from other known bacterial mdh genes. Appl Microbiol Biotechnol 2002; 59:665–671 [View Article] [PubMed]
    [Google Scholar]
  41. Hahn G, Kaup B, Bringer-Meyer S, Sahm H. A zinc-containing mannitol-2-dehydrogenase from Leuconostoc pseudomesenteroides ATCC 12291: purification of the enzyme and cloning of the gene. Arch Microbiol 2003; 179:101–107 [View Article] [PubMed]
    [Google Scholar]
  42. Sasaki Y, Laivenieks M, Zeikus JG. Lactobacillus reuteri ATCC 53608 mdh gene cloning and recombinant mannitol dehydrogenase characterization. Appl Microbiol Biotechnol 2005; 68:36–41 [View Article] [PubMed]
    [Google Scholar]
  43. Hettiarachchi A, Cnockaert M, Joossens M, Gekière A, Meeus I et al. The wild solitary bees Andrena vaga, Anthophora plumipes, Colletes cunicularius, and Osmia cornuta microbiota are host specific and dominated by endosymbionts and environmental microorganisms. Microb Ecol 2023a; 86:3013–3026 [View Article] [PubMed]
    [Google Scholar]
  44. Paoli PP, Donley D, Stabler D, Saseendranath A, Nicolson SW et al. Nutritional balance of essential amino acids and carbohydrates of the adult worker honeybee depends on age. Amino Acids 2014; 46:1449–1458 [View Article] [PubMed]
    [Google Scholar]
  45. Stabler D, Paoli PP, Nicolson SW, Wright GA. Nutrient balancing of the adult worker bumblebee (Bombus terrestris) depends on the dietary source of essential amino acids. J Exp Biol 2015; 218:793–802 [View Article] [PubMed]
    [Google Scholar]
  46. Rodriguez-R LM, Gunturu S, Harvey WT, Rosselló-Mora R, Tiedje JM et al. The microbial genomes atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res 2018; 46:W282–W288 [View Article] [PubMed]
    [Google Scholar]
  47. Wirth JS, Whitman WB. Phylogenomic analyses of a clade within the roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 2018; 68:2393–2411 [View Article] [PubMed]
    [Google Scholar]
  48. 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]
    [Google Scholar]
  49. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article] [PubMed]
    [Google Scholar]
  50. 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] [PubMed]
    [Google Scholar]
  51. Sun Z, Yu J, Dan T, Zhang W, Zhang H. Phylogenesis and evolution of lactic acid bacteria. In Zhang H, Cai Y. eds Lactic Acid Bacteria: Fundamentals and Practice Dordrecht: Springer Netherlands; 2014 [View Article]
    [Google Scholar]
  52. Vaudo AD, Tooker JF, Grozinger CM, Patch HM. Bee nutrition and floral resource restoration. Curr Opin Insect Sci 2015; 10:133–141 [View Article] [PubMed]
    [Google Scholar]
  53. Adler LS, Irwin RE, McArt SH, Vannette RL. Floral traits affecting the transmission of beneficial and pathogenic pollinator-associated microbes. Curr Opin Insect Sci 2021; 44:1–7 [View Article] [PubMed]
    [Google Scholar]
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