1887

Abstract

The genus is one of the most frequent bacterial inhabitants of flowers and a usual member of the insect microbiota worldwide. To date, there is only one publicly available genome, corresponding to the type strain of (8N4), which precludes a detailed analysis of intra-genus phylogenetic relationships. In this study, we obtained draft genomes of the type strains of the other species validly published to date (, and ) and 23 additional isolates of flower and insect origin. Isolate S61, retrieved from the nectar of an sp. flower collected in southern Spain, displayed low average nucleotide identity (ANI) and DNA–DNA hybridization (isDDH) values when compared with other members (≤86.5 and ≤29.8 %, respectively). Similarly, isolate JB07, which was obtained from the floral nectar of plants in Hawaii (USA) had ≤95.7 % ANI and ≤64.1 % isDDH with other isolates. Therefore, our results support the description of two new species for which we propose the names sp. nov. (type strain: S61=NCCB 100789=DSM 111181) and sp. nov. (JB07=NCCB 100888=LMG 32616). Additionally, some and isolates showed isDDH values<79 % with other conspecific isolates, which suggests that these species include subspecies for which we propose the names subsp. subsp. nov. (S256=CECT 8502=LMG 27956), subsp. subsp. nov. (FR72=NCCB 100898=LMG 32786), subsp. subsp. nov. (K24=NCCB 100924=LMG 32785), subsp. subsp. nov. (8N4 = DSM 24150 = LMG 26121) and subsp. subsp. nov. (B1A=NCCB 100810= DSM 111763), respectively. Finally, we present the first phylogenomic analysis of the genus and update the formal description of the species , , and based on new genomic and phenotypic information.

Funding
This study was supported by the:
  • Fundación BBVA
    • Principle Award Recipient: Clarade Vega
  • Ministerio de Ciencia e Innovación (Award RYC2018-023847-I)
    • Principle Award Recipient: SergioAlvarez-Perez
  • Deutsche Forschungsgemeinschaft (Award DFG, JU2856/2–2)
    • Principle Award Recipient: ApplicableNot
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/content/journal/ijsem/10.1099/ijsem.0.005777
2023-03-08
2024-04-20
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References

  1. Alvarez-Pérez S, Herrera CM. Composition, richness and nonrandom assembly of culturable bacterial-microfungal communities in floral nectar of Mediterranean plants. FEMS Microbiol Ecol 2013; 83:685–699 [View Article] [PubMed]
    [Google Scholar]
  2. Álvarez-Pérez S, Lievens B, Fukami T. Yeast-bacterium interactions: the next frontier in nectar research. Trends Plant Sci 2019; 24:393–401 [View Article]
    [Google Scholar]
  3. Bartlewicz J, Lievens B, Honnay O, Jacquemyn H. Microbial diversity in the floral nectar of Linaria vulgaris along an urbanization gradient. BMC Ecol 2016; 16:18 [View Article] [PubMed]
    [Google Scholar]
  4. Vega C, Álvarez‐Pérez S, Albaladejo RG, Steenhuisen S, Lachance M et al. The role of plant–pollinator interactions in structuring nectar microbial communities. J Ecol 2021; 109:3379–3395 [View Article]
    [Google Scholar]
  5. Lenaerts M, Pozo MI, Wäckers F, Van den Ende W, Jacquemyn H et al. Impact of microbial communities on floral nectar chemistry: potential implications for biological control of pest insects. Basic Appl Ecol 2016; 17:189–198 [View Article]
    [Google Scholar]
  6. Manirajan BA, Maisinger C, Ratering S, Rusch V, Schwiertz A et al. Diversity, specificity, co-occurrence and hub taxa of the bacterial-fungal pollen microbiome. FEMS Microbiol Ecol 2018; 94: [View Article] [PubMed]
    [Google Scholar]
  7. Ambika Manirajan B, Ratering S, Rusch V, Schwiertz A, Geissler-Plaum R et al. Bacterial microbiota associated with flower pollen is influenced by pollination type, and shows a high degree of diversity and species-specificity. Environ Microbiol 2016; 18:5161–5174 [View Article] [PubMed]
    [Google Scholar]
  8. Medlar AJ, Törönen P, Holm L. AAI-profiler: fast proteome-wide exploratory analysis reveals taxonomic identity, misclassification and contamination. Nucleic Acids Res 2018; 46:W479–W485 [View Article] [PubMed]
    [Google Scholar]
  9. Samuni-Blank M, Izhaki I, Laviad S, Bar-Massada A, Gerchman Y et al. The role of abiotic environmental conditions and herbivory in shaping bacterial community composition in floral nectar. PLoS One 2014; 9:e99107 [View Article]
    [Google Scholar]
  10. Sharaby Y, Rodríguez-Martínez S, Lalzar M, Halpern M, Izhaki I. Geographic partitioning or environmental selection: What governs the global distribution of bacterial communities inhabiting floral nectar?. Sci Total Environ 2020; 749:142305 [View Article]
    [Google Scholar]
  11. Alvarez-Pérez S, Herrera CM, de Vega C. Zooming-in on floral nectar: a first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiol Ecol 2012; 80:591–602 [View Article] [PubMed]
    [Google Scholar]
  12. Herrera CM. Scavengers that fit beneath a microscope lens. Ecology 2017; 98:2725–2726 [View Article] [PubMed]
    [Google Scholar]
  13. Herrera CM, Canto A, Pozo MI, Bazaga P. Inhospitable sweetness: nectar filtering of pollinator-borne inocula leads to impoverished, phylogenetically clustered yeast communities. Proc Biol Sci 2010; 277:747–754 [View Article] [PubMed]
    [Google Scholar]
  14. Lievens B, Hallsworth JE, Pozo MI, Belgacem ZB, Stevenson A et al. Microbiology of sugar-rich environments: diversity, ecology and system constraints. Environ Microbiol 2015; 17:278–298 [View Article] [PubMed]
    [Google Scholar]
  15. Morales-Poole JR, de Vega C, Tsuji K, Jacquemyn H, Junker RR et al. Sugar concentration, nitrogen availability, and phylogenetic factors determine the ability of Acinetobacter spp. and Rosenbergiella spp. to grow in floral nectar. Microb Ecol 2022 [View Article]
    [Google Scholar]
  16. Lenaerts M, Goelen T, Paulussen C, Herrera‐Malaver B, Steensels J et al. Nectar bacteria affect life history of a generalist aphid parasitoid by altering nectar chemistry. Funct Ecol 2017; 31:2061–2069 [View Article]
    [Google Scholar]
  17. Halpern M, Fridman S, Atamna-Ismaeel N, Izhaki I. Rosenbergiella nectarea gen. nov., sp. nov., in the family Enterobacteriaceae, isolated from floral nectar. Int J Syst Evol Microbiol 2013; 63:4259–4265 [View Article]
    [Google Scholar]
  18. Lenaerts M, Alvarez-Pérez S, de Vega C, Van Assche A, Johnson SD et al. Rosenbergiella australoborealis sp. nov., Rosenbergiella collisarenosi sp. nov. and Rosenbergiella epipactidis sp. nov., three novel bacterial species isolated from floral nectar. Syst Appl Microbiol 2014; 37:402–411 [View Article]
    [Google Scholar]
  19. 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]
  20. Soutar CD, Stavrinides J. Phylogenetic analysis supporting the taxonomic revision of eight genera within the bacterial order Enterobacterales. Int J Syst Evol Microbiol 2020; 70:6524–6530 [View Article] [PubMed]
    [Google Scholar]
  21. Laviad-Shitrit S, Izhaki I, Whitman WB, Shapiro N, Woyke T et al. Draft genome of Rosenbergiella nectarea strain 8N4T provides insights into the potential role of this species in its plant host. PeerJ 2020; 8:e8822 [View Article]
    [Google Scholar]
  22. Alvarez-Perez S, Baker LJ, Morris MM, Tsuji K, Sanchez VA et al. Acinetobacter pollinis sp. nov., Acinetobacter baretiae sp. nov. and Acinetobacter rathckeae sp. nov., isolated from floral nectar and honey bees. Int J Syst Evol Microbiol 2021; 71: [View Article]
    [Google Scholar]
  23. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  24. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucl Acids Symp Ser 1999; 41:95–98
    [Google Scholar]
  25. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
    [Google Scholar]
  26. Lefort V, Longueville JE, Gascuel O. SMS: Smart Model Selection in PhyML. Mol Biol Evol 2017; 34:2422–2424 [View Article] [PubMed]
    [Google Scholar]
  27. 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]
    [Google Scholar]
  28. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article]
    [Google Scholar]
  29. 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]
    [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article] [PubMed]
    [Google Scholar]
  34. van Heeringen SJ. genomepy: download genomes the easy way. JOSS 2017; 2:320 [View Article]
    [Google Scholar]
  35. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  36. 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]
  37. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  38. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 2009; 106:19126–19131 [View Article]
    [Google Scholar]
  39. 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]
  40. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  41. Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 2018; 35:518–522 [View Article]
    [Google Scholar]
  42. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article]
    [Google Scholar]
  43. Kim J, Kim D, Chun J. UBCG2: up-to-date bacterial core genes and pipeline for phylogenomic analysis. J Microbiol 2021; 59:609–615 [View Article]
    [Google Scholar]
  44. Álvarez-Pérez S, Lievens B, Jacquemyn H, Herrera CM. Acinetobacter nectaris sp. nov. and Acinetobacter boissieri sp. nov., isolated from floral nectar of wild Mediterranean insect-pollinated plants. Int J Syst Evol Microbiol 2013; 63:1532–1539 [View Article]
    [Google Scholar]
  45. Halpern M, Fridman S, Aizenberg-Gershtein Y, Izhaki I. Transfer of Pseudomonas flectens Johnson 1956 to Phaseolibacter gen. nov., in the family Enterobacteriaceae, as Phaseolibacter flectens gen. nov., comb. nov. Int J Syst Evol Microbiol 2013; 63:268–273 [View Article]
    [Google Scholar]
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