1887

Abstract

The honey bee gut microbiota contains many bacterial lineages that are specific to this ecosystem. , raised across the Asian continent, is of great significance to the maintenance and development of ecology and agriculture in Asia. Here, we report the isolation and characterization of strain QZS01 from the gut of from Pingwu County, Sichuan Province, PR China. The results of phylogenetic analysis based on 16S rRNA sequences showed that strain QZS01 forms a monophyletic group together with clone sequences derived from variable insect hosts, and it shows 92% sequence similarity to its closest relative, . Strain QZS01 possesses a reduced genome (3.3 Mbp; G+C content, 38.05 mol%) compared to all other species, and the whole-genome based phylogenetic reconstruction showed that strain QZS01 represents a novel genus within the family . Strain QZS01 is a Gram-stain-negative facultative anaerobe. It grows on brain heart infusion agar and the energy sources utilized for growth are very limited. Based on the results of genotypic and phenotypic analyses, we propose a novel genus and species, gen. nov., sp. nov., with the type strain QZS01 (=CGMCC 1.13498=KCTC 62495).

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/content/journal/ijsem/10.1099/ijsem.0.003731
2019-09-27
2019-10-18
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References

  1. Winsor GL, Griffiths EJ, Lo R, Dhillon BK, Shay JA et al. Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database. Nucleic Acids Res 2016;44:D646–D653 [CrossRef][PubMed]
    [Google Scholar]
  2. Gellatly SL, Hancock RE. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog Dis 2013;67:159–173 [CrossRef][PubMed]
    [Google Scholar]
  3. Flury P, Vesga P, Dominguez-Ferreras A, Tinguely C, Ullrich CI et al. Persistence of root-colonizing Pseudomonas protegens in herbivorous insects throughout different developmental stages and dispersal to new host plants. Isme J 2019;13:860–872 [CrossRef][PubMed]
    [Google Scholar]
  4. Vodovar N, Vinals M, Liehl P, Basset A, Degrouard J et al. Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc Natl Acad Sci USA 2005;102:11414–11419 [CrossRef][PubMed]
    [Google Scholar]
  5. Zheng H, Nishida A, Kwong WK, Koch H, Engel P et al. Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont Gilliamella apicola. MBio 2016;7:e0132616 [CrossRef][PubMed]
    [Google Scholar]
  6. Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc Natl Acad Sci USA 2017;114:4775–4780 [CrossRef][PubMed]
    [Google Scholar]
  7. Kwong WK, Moran NA. Evolution of host specialization in gut microbes: the bee gut as a model. Gut Microbes 2015;6:214–220 [CrossRef][PubMed]
    [Google Scholar]
  8. Hepburn HR, Radloff SE. Honeybees of Asia. In Hepburn HR, Radloff SE. (editors) Heidelberg: Springer-Verlag Berlin Heidelberg; 2011; pp.1–669
  9. Tan K, Yang S, Wang ZW, Radloff SE, Oldroyd BP. Differences in foraging and broodnest temperature in the honey bees Apis cerana and A. mellifera. Apidologie 2012;43:618–623 [CrossRef]
    [Google Scholar]
  10. Kwong WK, Medina LA, Koch H, Sing KW, Soh EJY et al. Dynamic microbiome evolution in social bees. Sci Adv 2017;3:e1600513 [CrossRef][PubMed]
    [Google Scholar]
  11. Spurr AR. A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 1969;26:31–43 [CrossRef][PubMed]
    [Google Scholar]
  12. Rojo F. Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiol Rev 2010;34:658–684 [CrossRef][PubMed]
    [Google Scholar]
  13. Mccutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 2012;10:13–26 [CrossRef]
    [Google Scholar]
  14. Goodfellow M, Minnikin DE. Nocardioform bacteria. Annu Rev Microbiol 1977;31:159–180 [CrossRef][PubMed]
    [Google Scholar]
  15. Minnikin DE, O'Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984;2:233–241 [CrossRef]
    [Google Scholar]
  16. Komagata K, Suzuki K. Lipids and cell-wall analysis in bacterial systematics. Methods Microbiol 1988;19:161–207
    [Google Scholar]
  17. Winnepenninckx B, Backeljau T, de Wachter R. Extraction of high molecular weight DNA from molluscs. Trends Genet 1993;9:407[PubMed]
    [Google Scholar]
  18. Zheng H, Dietrich C, Brune A. Genome analysis of Endomicrobium proavitum suggests loss and gain of relevant functions during the evolution of intracellular symbionts. Appl Environ Microbiol 2017;83:e0065617 [CrossRef][PubMed]
    [Google Scholar]
  19. Moran NA, Bennett GM. The tiniest tiny genomes. Annu Rev Microbiol 2014;68:195–215 [CrossRef][PubMed]
    [Google Scholar]
  20. Tatusova T, Dicuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016;44:6614–6624 [CrossRef][PubMed]
    [Google Scholar]
  21. Lane DJ. 16S/23S rRNA sequencing. In Stackebrandt E, Goodfellow M. (editors) Nucleic acids techniques in bacterial systematics Chichester: John Wiley & Sons; 1991; pp.115–175
    [Google Scholar]
  22. Babendreier D, Joller D, Romeis J, Bigler F, Widmer F. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol Ecol 2007;59:600–610 [CrossRef][PubMed]
    [Google Scholar]
  23. Koch H, Schmid-Hempel P. Bacterial communities in central European bumblebees: low diversity and high specificity. Microb Ecol 2011;62:121–133 [CrossRef][PubMed]
    [Google Scholar]
  24. Chu CC, Spencer JL, Curzi MJ, Zavala JA, Seufferheld MJ. Gut bacteria facilitate adaptation to crop rotation in the western corn rootworm. Proc Natl Acad Sci USA 2013;110:11917–11922 [CrossRef][PubMed]
    [Google Scholar]
  25. Estes AM, Hearn DJ, Snell-Rood EC, Feindler M, Feeser K et al. Brood ball-mediated transmission of microbiome members in the dung beetle, Onthophagus taurus (Coleoptera: Scarabaeidae). PLoS One 2013;8:e79061 [CrossRef][PubMed]
    [Google Scholar]
  26. Lehman RM, Lundgren JG, Petzke LM. Bacterial communities associated with the digestive tract of the predatory ground beetle, Poecilus chalcites, and their modification by laboratory rearing and antibiotic treatment. Microb Ecol 2009;57:349–358 [CrossRef][PubMed]
    [Google Scholar]
  27. Anderson KE, Russell JA, Moreau CS, Kautz S, Sullam KE et al. Highly similar microbial communities are shared among related and trophically similar ant species. Mol Ecol 2012;21:2282–2296 [CrossRef][PubMed]
    [Google Scholar]
  28. Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ et al. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci USA 2009;106:21236–21241 [CrossRef][PubMed]
    [Google Scholar]
  29. Gomila M, Peña A, Mulet M, Lalucat J, García-Valdés E. Phylogenomics and systematics in Pseudomonas. Front Microbiol 2015;6:214 [CrossRef][PubMed]
    [Google Scholar]
  30. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  31. Mulet M, Gomila M, Scotta C, Sánchez D, Lalucat J et al. Concordance between whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry and multilocus sequence analysis approaches in species discrimination within the genus Pseudomonas. Syst Appl Microbiol 2012;35:455–464 [CrossRef][PubMed]
    [Google Scholar]
  32. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013;4:2304 [CrossRef][PubMed]
    [Google Scholar]
  33. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009;106:19126–19131 [CrossRef][PubMed]
    [Google Scholar]
  34. 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 [CrossRef][PubMed]
    [Google Scholar]
  35. Jensen HL. Azotobacter Macrocytogenes n. sp., a nitrogen-fixing bacterium resistant to acid reaction. Acta Agriculturae Scandinavica 1955;5:280–294 [CrossRef]
    [Google Scholar]
  36. Holmes B, Steigerwalt AG, Weaver RE, Brenner DJ. Chryseomonas polytricha gen. nov., sp. nov., a Pseudomonas-Like Organism from Human Clinical Specimens and Formerly Known as Group Ve-1. Int J Syst Bacteriol 1986;36:161–165 [CrossRef]
    [Google Scholar]
  37. Holmes B, Steigerwalt AG, Weaver RE, Brenner DJ. Chryseomonas luteola comb. nov. and Flavimonas oryzihabitans gen. nov., comb. nov., Pseudomonas-Like Species from Human Clinical Specimens and Formerly Known, Respectively, as Groups Ve-1 and Ve-2. Int J Syst Bacteriol 1987;37:245–250 [CrossRef]
    [Google Scholar]
  38. Drobish AM, Emery BD, Whitney AM, Lauer AC, Metcalfe MG et al. Oblitimonas alkaliphila gen. nov., sp. nov., in the family Pseudomonadaceae, recovered from a historical collection of previously unidentified clinical strains. Int J Syst Evol Microbiol 2016;66:3063–3070 [CrossRef][PubMed]
    [Google Scholar]
  39. Wang H, Zheng T, Hill RT, Hu X. Permianibacter aggregans gen. nov., sp. nov., a bacterium of the family Pseudomonadaceae capable of aggregating potential biofuel-producing microalgae. Int J Syst Evol Microbiol 2014;64:3503–3507 [CrossRef][PubMed]
    [Google Scholar]
  40. Xiao YP, Hui W, Wang Q, Roh SW, Shi XQ et al. Pseudomonas caeni sp. nov., a denitrifying bacterium isolated from the sludge of an anaerobic ammonium-oxidizing bioreactor. Int J Syst Evol Microbiol 2009;59:2594–2598 [CrossRef][PubMed]
    [Google Scholar]
  41. Clark LL, Dajcs JJ, Mclean CH, Bartell JG, Stroman DW. Pseudomonas otitidis sp. nov., isolated from patients with otic infections. Int J Syst Evol Microbiol 2006;56:709–714 [CrossRef][PubMed]
    [Google Scholar]
  42. Gibello A, Vela AI, Martín M, Mengs G, Alonso PZ et al. Pseudomonas composti sp. nov., isolated from compost samples. Int J Syst Evol Microbiol 2011;61:2962–2966 [CrossRef][PubMed]
    [Google Scholar]
  43. Yumoto I, Yamazaki K, Hishinuma M, Nodasaka Y, Suemori A et al. Pseudomonas alcaliphila sp. nov., a novel facultatively psychrophilic alkaliphile isolated from seawater. Int J Syst Evol Microbiol 2001;51:349–355 [CrossRef][PubMed]
    [Google Scholar]
  44. Goto M, Kuwata H. Rhizobacter daucus gen. nov., sp. nov., the causal agent of carrot bacterial gall. Int J Syst Bacteriol 1988;38:233–239 [CrossRef]
    [Google Scholar]
  45. Wei L, Si M, Long M, Zhu L, Li C et al. Rhizobacter bergeniae sp. nov., isolated from the root of Bergenia scopulosa. Int J Syst Evol Microbiol 2015;65:479–484 [CrossRef][PubMed]
    [Google Scholar]
  46. Austin DA, Moss MO. Numerical taxonomy of red-pigmented bacteria isolated from a lowland river, with the description of a new taxon, Rugamonas rubra gen. nov., sp. nov. Microbiology 1986;132:1899–1909 [CrossRef]
    [Google Scholar]
  47. Hespell RB. Serpens flexibilis gen. nov., sp. nov., an unusually flexible, lactate-oxidizing bacterium. Int J Syst Bacteriol 1977;27:371–381 [CrossRef]
    [Google Scholar]
  48. Tan WB, Jiang Z, Chen C, Yuan Y, Gao LF et al. Thiopseudomonas denitrificans gen. nov., sp. nov., isolated from anaerobic activated sludge. Int J Syst Evol Microbiol 2015;65:225–229 [CrossRef][PubMed]
    [Google Scholar]
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