1887

Abstract

Cephalotes ‘turtle’ ants host a core group of gut–associated symbionts, but their potential contributions to ant nutrition and disease resistance remain uncharacterized in vitro. To gain a better understanding of the metabolic capability of core symbionts belonging to the Burkholderiales , we cultivated and characterized strain CAG32 from the guts of Cephalotes rohweri ants. Strain CAG32 was rod-shaped, Gram-stain-negative, motile and formed pale-white colonies on trypticase soy agar. Optimum growth occurred under an atmosphere of 20 % O2 supplemented with 1 % CO2. Strain CAG32 grew under NaCl concentrations of 0–2.0 %, temperatures of 23–47 °C and pH values of 4.0–8.0, and was capable of producing n-butyric acid and degrading carbohydrates for growth. The G+C content of the genomic DNA was 59.2±0.6 mol% and the major fatty acids were C16 : 0, C16 : 1 ω7c/C16  : 1 ω6c, C17 : 0 cylcopropane, C12 : 0 and C14 : 0 3-OH/C16 : 1 iso I. The only respiratory quinone detected was ubiquinone-8 (Q-8) and the major polar lipids were phosphatidylethanolamine, phosphatidylglycerol and diphosphatidylglycerol. Based on phylogenetic analysis of the 16S rRNA gene sequence, strain CAG32 shared 96.9 % nucleotide similarity with its closest cultivated neighbours Bordetella petrii Se-1111R and Bordetella bronchiseptica ATCC 19395. This, combined with differences in the phenotypic and biochemical profile from neighbouring strains, warrants the classification of strain CAG32 as representing a novel species of a new genus within the Burkholderiales family Alcaligenaceae . The name Saccharedens versatilis gen. nov., sp. nov. is proposed. The type strain of Saccharedens versatilis is CAG32 (=NCIMB 15010=DSM 100909).

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2017-02-24
2019-12-09
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References

  1. Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 2004;49:71–92 [CrossRef][PubMed]
    [Google Scholar]
  2. Engel P, Moran NA. The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev 2013;37:699–735 [CrossRef][PubMed]
    [Google Scholar]
  3. McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 2013;110:3229–3236 [CrossRef][PubMed]
    [Google Scholar]
  4. Price SL, Powell S, Kronauer DJC, Tran LAP, Pierce NE et al. Renewed diversification is associated with new ecological opportunity in the Neotropical turtle ants. J Evol Biol 2014;27:242–258 [CrossRef][PubMed]
    [Google Scholar]
  5. 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]
  6. Jaffe K, Caetano FH, Sánchez P, Hernández JV, Caraballo L et al. Sensitivity of ant (Cephalotes) colonies and individuals to antibiotics implies feeding symbiosis with gut microorganisms. Can J Zool 2001;79:1120–1124 [CrossRef]
    [Google Scholar]
  7. 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]
  8. Hu Y, Łukasik P, Moreau CS, Russell JA. Correlates of gut community composition across an ant species (Cephalotes varians) elucidate causes and consequences of symbiotic variability. Mol Ecol 2014;23:1284–1300 [CrossRef][PubMed]
    [Google Scholar]
  9. Kautz S, Rubin BER, Russell JA, Moreau CS. Surveying the microbiome of ants: comparing 454 pyrosequencing with traditional methods to uncover bacterial diversity. Appl Environ Microbiol 2013;79:525–534 [CrossRef][PubMed]
    [Google Scholar]
  10. Lanan MC, Rodrigues PAP, Agellon A, Jansma P, Wheeler DE. A bacterial filter protects and structures the gut microbiome of an insect. ISME J 2016;10:1866–1876 [CrossRef][PubMed]
    [Google Scholar]
  11. Sanders JG, Powell S, Kronauer DJC, Vasconcelos HL, Frederickson ME et al. Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Mol Ecol 2014;23:1268–1283 [CrossRef][PubMed]
    [Google Scholar]
  12. Lin JY, Hobson WJ, Wertz JT. Ventosimonas gracilis gen. nov., sp. nov., a member of the Gammaproteobacteria isolated from Cephalotes varians ant guts representing a new family, Ventosimonadaceae fam. nov., within the order 'Pseudomonadales'. Int J Syst Evol Microbiol 2016;66:2869–2875 [CrossRef][PubMed]
    [Google Scholar]
  13. Lin JY, Russell JA, Sanders JG, Wertz JT. Cephaloticoccus gen. nov., a new genus of 'Verrucomicrobia' containing two novel species isolated from Cephalotes ant guts. Int J Syst Evol Microbiol 2016;66:3034–3040 [CrossRef][PubMed]
    [Google Scholar]
  14. Baker GC, Smith JJ, Cowan DA. Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 2003;55:541–555 [CrossRef][PubMed]
    [Google Scholar]
  15. Wertz JT, Breznak JA. Stenoxybacter acetivorans gen. nov., sp. nov., an acetate-oxidizing obligate microaerophile among diverse O2–consuming bacteria from termite guts. Appl Environ Microbiol 2007;73:6819–6828 [CrossRef][PubMed]
    [Google Scholar]
  16. Breznak JA, Costilow RN. Physicochemical factors in growth. In Marzluf GA, Reddy CA, Beveridge TJ, Schmidt TM, Snyder LR. et al. (editors) Methods Gen Mol Microbiol, 3rd ed. 2007; pp.309–329
    [Google Scholar]
  17. Wertz JT, Breznak JA. Physiological ecology of Stenoxybacter acetivorans, an obligate microaerophile in termite guts. Appl Environ Microbiol 2007;73:6829–6841 [CrossRef][PubMed]
    [Google Scholar]
  18. Tholen A, Brune A. Impact of oxygen on metabolic fluxes and in situ rates of reductive acetogenesis in the hindgut of the wood-feeding termite Reticulitermes flavipes. Environ Microbiol 2000;2:436–449 [CrossRef][PubMed]
    [Google Scholar]
  19. Zhao G, Nyman M, Jönsson JA. Rapid determination of short-chain fatty acids in colonic contents and faeces of humans and rats by acidified water-extraction and direct-injection gas chromatography. Biomed Chromatogr 2006;20:674–682 [CrossRef][PubMed]
    [Google Scholar]
  20. Tindall BJ, Sikorski J, Smibert RA, Krieg NR. Phenotypic characterization and the principles of comparative systematics. In Marzluf GA, Reddy CA, Beveridge TJ, Schmidt TM, Snyder LR. et al. (editors) Methods Gen Mol Microbiol, 3rd ed.. American Society of Microbiology; 2007; pp.330–393
    [Google Scholar]
  21. Mesbah M, Premachandran U, Whitman WB. Precise measurement of the G+C content of deoxyribonucleic acid by high–performance liquid chromatography. Int J Syst Evol Microbiol 1989;39:159–167
    [Google Scholar]
  22. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215:403–410 [CrossRef][PubMed]
    [Google Scholar]
  23. Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823–1829 [CrossRef][PubMed]
    [Google Scholar]
  24. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013;30:2725–2729 [CrossRef][PubMed]
    [Google Scholar]
  25. Vandamme PA. Proposal of Verticiella gen. nov. as the replacement for the illegitimate prokaryotic genus name Verticia Vandamme 2015. Int J Syst Evol Microbiol 2016;66:5099–5100 [CrossRef][PubMed]
    [Google Scholar]
  26. Vandamme PA, Peeters C, Cnockaert M, Inganäs E, Falsen E et al. Bordetella bronchialis sp. nov., Bordetella flabilis sp. nov. and Bordetella sputigena sp. nov., isolated from human respiratory specimens, and reclassification of Achromobacter sediminum Zhang et al. 2014 as Verticia sediminum gen. nov., comb. nov. Int J Syst Evol Microbiol 2015;65:3674–3682 [CrossRef][PubMed]
    [Google Scholar]
  27. Von Wintzingerode F, Schattke A, Siddiqui RA, Rösick U, Göbel UB et al. Bordetella petrii sp. nov., isolated from an anaerobic bioreactor, and emended description of the genus Bordetella. Int J Syst Evol Microbiol 2001;51:1257–1265 [CrossRef][PubMed]
    [Google Scholar]
  28. Skerman VBD, McGowan V, Sneath PHA. Approved lists of bacterial names. Int J Syst Evol Microbiol 1980;30:225–420 [CrossRef]
    [Google Scholar]
  29. Austin B. The family Alcaligenaceae. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. et al. (editors) The Prokaryotes Berlin Heidelberg: Springer; 2014; pp.729–757[CrossRef]
    [Google Scholar]
  30. Weiss A. The genus Bordetella. In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. et al. (editors) The Prokaryotes New York: Springer; 2006; pp.648–674[CrossRef]
    [Google Scholar]
  31. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014;64:346–351 [CrossRef][PubMed]
    [Google Scholar]
  32. Park MS, Park Y-J, Jung JY, Lee SH, Park W et al. Pusillimonas harenae sp. nov., isolated from a sandy beach, and emended description of the genus Pusillimonas. Int J Syst Evol Microbiol 2011;61:2901–2906 [CrossRef][PubMed]
    [Google Scholar]
  33. Daligault HE, Davenport KW, Minogue TD, Bishop-Lilly KA, Bruce DC et al. Draft genome assembly of Bordetella bronchiseptica ATCC 10580, a historical canine clinical isolate. Genome Announc 2014;2:e00916-14 [CrossRef][PubMed]
    [Google Scholar]
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