1887

Abstract

A novel bacterium designated G55GP and pertaining to the family was isolated from the gut of the Madagascar hissing cockroach . The Gram-negative cells were rod-shaped and non-motile. The complete 16S rRNA sequence of the strain G55GP showed the highest pairwise similarity to CFN-Cf-55T (95.35 %), suggesting it represents a potential new genus of the family . Phylogenetic analysis based on 16S rRNA gene and 106 orthologous housekeeping protein sequences revealed that G55GP forms a monophyletic clade with the genus , which thus far has also been isolated exclusively from insects. The G55GP genome size was 2.70 Mbp, and the G+C content was 45.4 mol%, which is lower than most acetic acid bacteria (51–68 mol%) but comparable to AH83 (45.1 mol%) and higher than A911 (36.8 mol%). Overall genome relatedness indices based on gene and protein sequences strongly supported the assignment of G55GP to a new genus within the family . The percentage of conserved proteins, which is a useful metric for genus differentiation, was below 54 % when comparing G55GP to type strains of acetic acid bacteria, thus strongly supporting our hypothesis that G55GP is a member of a yet-undescribed genus. The fatty acid composition of G55GP differed from that of closely related acetic acid bacteria, particularly given the presence of C 9/11 and the absence of C and C 2-OH fatty acids. Strain G55GP also differed in terms of metabolic features such as its ability to produce acid from -mannitol, and its inability to produce acetic acid from ethanol or to oxidize glycerol to dihydroxyacetone. Based on the results of combined genomic, phenotypic and phylogenetic characterizations, isolate G55GP (=LMG 31394=DSM 111244) is considered to represent a new species in a new genus, for which we propose the name gen. nov., sp. nov.

Funding
This study was supported by the:
  • JuanDavid Guzman , Alexander von Humboldt-Stiftung
  • AndreasVilcinskas , LOEWE Zentrum AdRIA
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004666
2021-02-02
2021-02-26
Loading full text...

Full text loading...

References

  1. Hördt A, López MG, Meier-Kolthoff JP, Schleuning M, Weinhold L-M et al. Analysis of 1000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria . Front Microbiol 2020; 11: 468 [CrossRef] [PubMed]
    [Google Scholar]
  2. Komagata K, Iino T, Yamada Y. The family Acetobacteraceae. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. (editors) The Prokaryotes: Alphaproteobacteria and Betaproteobacteria Berlin, Heidelberg: Springer Berlin Heidelberg; 2014 pp 3 78
    [Google Scholar]
  3. Malimas T, HTL V, Muramatsu Y, Yukphan P, Tanasupawat S. Systematics of acetic acid bacteria. In Sengun IY. editor Acetic Acid Bacteria Fundamentals and Food Applications Boca Raton, FL: CRC Press; 2016 pp 3 43
    [Google Scholar]
  4. Sievers M, Swings J. Acetobacteraceae. Bergey’s Manual of Systematics of Archaea and Bacteria 2015 pp 1 20
    [Google Scholar]
  5. Kersters K, Lisdiyanti P, Komagata K, Swings J. The family Acetobacteraceae: the genera Acetobacter, Acidomonas, Asaia, Gluconacetobacter, Gluconobacter, and Kozakia . In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E. (editors) The Prokaryotes: Volume 5: Proteobacteria: Alpha and Beta Subclasses New York, NY: Springer New York; 2006 pp 163 200
    [Google Scholar]
  6. Yukphan P, Malimas T, Muramatsu Y, Takahashi M, Kaneyasu M et al. Ameyamaea chiangmaiensis gen. nov., sp. nov., an acetic acid bacterium in the alpha-proteobacteria. Biosci Biotechnol Biochem 2009; 73: 2156 2162 [CrossRef] [PubMed]
    [Google Scholar]
  7. Yukphan P, Malimas T, Muramatsu Y, Potacharoen W, Tanasupawat S et al. Neokomagataea gen. nov., with descriptions of Neokomagataea thailandica sp. nov. and Neokomagataea tanensis sp. nov., osmotolerant acetic acid bacteria of the α-Proteobacteria. Biosci Biotechnol Biochem 2011; 75: 419 426 [CrossRef] [PubMed]
    [Google Scholar]
  8. Yamada Y, Yukphan P, Lan Vu HT, Muramatsu Y, Ochaikul D et al. Description of Komagataeibacter gen. nov., with proposals of new combinations (Acetobacteraceae). J Gen Appl Microbiol 2012; 58: 397 404 [CrossRef] [PubMed]
    [Google Scholar]
  9. Ramírez-Bahena MH, Tejedor C, Martín I, Velázquez E, Peix A. Endobacter medicaginis gen. nov., sp. nov., isolated from alfalfa nodules in an acidic soil. Int J Syst Evol Microbiol 2013; 63: 1760 1765 [CrossRef] [PubMed]
    [Google Scholar]
  10. Thi Lan Vu H, Yukphan P, Chaipitakchonlatarn W, Malimas T, Muramatsu Y et al. Nguyenibacter vanlangensis gen. nov., sp. nov., an unusual acetic acid bacterium in the α-Proteobacteria. J Gen Appl Microbiol 2013; 59: 153 166 [CrossRef] [PubMed]
    [Google Scholar]
  11. Malimas T, Chaipitakchonlatarn W, Thi Lan Vu H, Yukphan P, Muramatsu Y et al. Swingsia samuiensis gen. nov., sp. nov., an osmotolerant acetic acid bacterium in the α-Proteobacteria. J Gen Appl Microbiol 2013; 59: 375 384 [CrossRef] [PubMed]
    [Google Scholar]
  12. Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G et al. Acetic acid bacteria, newly emerging symbionts of insects. Appl Environ Microbiol 2010; 76: 6963 6970 [CrossRef] [PubMed]
    [Google Scholar]
  13. Roh SW, Nam Y-D, Chang H-W, Kim K-H, Kim M-S et al. Phylogenetic characterization of two novel commensal bacteria involved with innate immune homeostasis in Drosophila melanogaster . Appl Environ Microbiol 2008; 74: 6171 6177 [CrossRef] [PubMed]
    [Google Scholar]
  14. Oren A, Garrity GM. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2019; 69: 1247 1250 [CrossRef] [PubMed]
    [Google Scholar]
  15. 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 [CrossRef] [PubMed]
    [Google Scholar]
  16. Corby-Harris V, Snyder LA, Schwan MR, Maes P, McFrederick QS et al. Origin and effect of alpha 2.2 Acetobacteraceae in honey bee larvae and description of Parasaccharibacter apium gen. nov., sp. nov. Appl Environ Microbiol 2014; 80: 7460 7472 [CrossRef] [PubMed]
    [Google Scholar]
  17. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of prokaryotic names with standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70: 5607 5612 [CrossRef] [PubMed]
    [Google Scholar]
  18. Li L, Praet J, Borremans W, Nunes OC, Manaia CM et al. Bombella intestini gen. nov., sp. nov., an acetic acid bacterium isolated from bumble bee crop. Int J Syst Evol Microbiol 2015; 65: 267 273 [CrossRef]
    [Google Scholar]
  19. Li L, Praet J, Borremans W, Nunes OC, Manaia CM et al. Bombella intestini gen. nov., sp. nov., an acetic acid bacterium isolated from bumble bee crop. Int J Syst Evol Microbiol 2015; 65: 267 273 [CrossRef] [PubMed]
    [Google Scholar]
  20. Newton ILG, Roeselers G. The effect of training set on the classification of honey bee gut microbiota using the naïve Bayesian classifier. BMC Microbiol 2012; 12: 221 [CrossRef] [PubMed]
    [Google Scholar]
  21. Guzman J, Vilcinskas A. Bacteria associated with cockroaches: health risk or biotechnological opportunity?. Appl Microbiol Biotechnol 2020; 104: 10369 10387 [CrossRef] [PubMed]
    [Google Scholar]
  22. Li J, Dong J-D, Yang J, Luo X-M, Zhang S. Detection of polyketide synthase and nonribosomal peptide synthetase biosynthetic genes from antimicrobial coral-associated actinomycetes. Antonie van Leeuwenhoek 2014; 106: 623 635 [CrossRef] [PubMed]
    [Google Scholar]
  23. Packeiser H, Lim C, Balagurunathan B, Wu J, Zhao H. An extremely simple and effective colony PCR procedure for bacteria, yeasts, and microalgae. Appl Biochem Biotechnol 2013; 169: 695 700 [CrossRef] [PubMed]
    [Google Scholar]
  24. 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 [CrossRef] [PubMed]
    [Google Scholar]
  25. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30: 772 780 [CrossRef] [PubMed]
    [Google Scholar]
  26. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312 1313 [CrossRef] [PubMed]
    [Google Scholar]
  27. Aberer AJ, Kobert K, Stamatakis A. ExaBayes: massively parallel Bayesian tree inference for the whole-genome era. Mol Biol Evol 2014; 31: 2553 2556 [CrossRef] [PubMed]
    [Google Scholar]
  28. Salvà Serra F, Salvà-Serra F, Svensson-Stadler L, Busquets A, Jaén-Luchoro D et al. A protocol for extraction and purification of high-quality and quantity bacterial DNA applicable for genome sequencing: a modified version of the Marmur procedure. Protoc Exch 2018; 084: [CrossRef]
    [Google Scholar]
  29. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13: e1005595 [CrossRef] [PubMed]
    [Google Scholar]
  30. Wick RR, Schultz MB, Zobel J, Holt KE. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 2015; 31: 3350 3352 [CrossRef] [PubMed]
    [Google Scholar]
  31. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30: 2068 2069 [CrossRef] [PubMed]
    [Google Scholar]
  32. Lee I, Chalita M, Ha S-M, Na S-I, Yoon S-H et al. ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int J Syst Evol Microbiol 2017; 67: 2053 2057 [CrossRef] [PubMed]
    [Google Scholar]
  33. Ankenbrand MJ, Keller A. bcgTree: automatized phylogenetic tree building from bacterial core genomes. Genome 2016; 59: 783 791 [CrossRef] [PubMed]
    [Google Scholar]
  34. Bonilla-Rosso G, Paredes Juan C, Das S, Ellegaard K, Emery O. Acetobacteraceae in the honey bee gut comprise two distant clades with diverging metabolism and ecological niches. bioRxiv 2019; 861260:
    [Google Scholar]
  35. Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66: 1100 1103 [CrossRef] [PubMed]
    [Google Scholar]
  36. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14: 60 [CrossRef] [PubMed]
    [Google Scholar]
  37. 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 [CrossRef] [PubMed]
    [Google Scholar]
  38. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe 2014; 9: 111 118 [CrossRef]
    [Google Scholar]
  39. Luo C, Rodriguez-R LM, Konstantinidis KT. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 2014; 42: e73 [CrossRef] [PubMed]
    [Google Scholar]
  40. Ram JL, Karim AS, Sendler ED, Kato I. Strategy for microbiome analysis using 16S rRNA gene sequence analysis on the Illumina sequencing platform. Syst Biol Reprod Med 2011; 57: 162 170 [CrossRef] [PubMed]
    [Google Scholar]
  41. Cardoso A, Gómez-Zurita J. Food resource sharing of alder leaf beetle specialists (Coleoptera: Chrysomelidae) as potential insect-plant interface for horizontal transmission of endosymbionts. Environ Entomol 2020; 49: 1402 1414 [CrossRef] [PubMed]
    [Google Scholar]
  42. De Cock M, Virgilio M, Vandamme P, Bourtzis K, De Meyer M et al. Comparative microbiomics of tephritid frugivorous pests (Diptera: Tephritidae) from the field: a tale of high variability across and within species. Front Microbiol 2020; 11: 11 [CrossRef] [PubMed]
    [Google Scholar]
  43. Gong Q, Cao LJ, Chen JC, Gong YJ, DQ P. Similar gut bacterial microbiota in two fruit-feeding moth pests collected from different host species and locations. bioRxiv 2020
    [Google Scholar]
  44. Kounatidis I, Crotti E, Sapountzis P, Sacchi L, Rizzi A et al. Acetobacter tropicalis is a major symbiont of the olive fruit fly (Bactrocera oleae). Appl Environ Microbiol 2009; 75: 3281 3288 [CrossRef] [PubMed]
    [Google Scholar]
  45. Smith EA, Anderson KE, Corby-Harris V, McFrederick QS, Newton ILG. Reclassification of seven honey bee symbiont strains as Bombella apis . bioRxiv 2020.05.06.081802
    [Google Scholar]
  46. Servín-Garcidueñas LE, Sánchez-Quinto A, Martínez-Romero E. Draft genome sequence of Commensalibacter papalotli MX01, a symbiont identified from the guts of overwintering monarch butterflies. Genome Announc 2014; 2: e00128 00114 [CrossRef] [PubMed]
    [Google Scholar]
  47. Siozios S, Moran J, Chege M, Hurst GDD, Paredes JC. Complete reference genome assembly for Commensalibacter sp. Strain AMU001, an acetic acid bacterium isolated from the gut of honey bees. Microbiol Resour Announc 2019; 8: 03 01 2019 [CrossRef] [PubMed]
    [Google Scholar]
  48. Cleenwerck I, Vandemeulebroecke K, Janssens D, Swings J. Re-examination of the genus Acetobacter, with descriptions of Acetobacter cerevisiae sp. nov. and Acetobacter malorum sp. nov. Int J Syst Evol Microbiol 2002; 52: 1551 1558 [CrossRef] [PubMed]
    [Google Scholar]
  49. Yamada Y, Katsura K, Kawasaki H, Widyastuti Y, Saono S et al. Asaia bogorensis gen. nov., sp. nov., an unusual acetic acid bacterium in the alpha-Proteobacteria. Int J Syst Evol Microbiol 2000; 50 Pt 2: 823 829 [CrossRef] [PubMed]
    [Google Scholar]
  50. Swings J. Phenotypic identification of acetic acid bacteria. Identification methods in applied and environmental microbiology (the Society for applied bacteriology technical series no 29). 1992 103 110
  51. Dumolin C, Aerts M, Verheyde B, Schellaert S, Vandamme T et al. Introducing SPeDE: high-throughput Dereplication and accurate determination of microbial diversity from matrix-assisted laser desorption-ionization time of flight mass spectrometry data. mSystems 2019; 4: e00437 00419 [CrossRef] [PubMed]
    [Google Scholar]
  52. Yamashita S-I, Uchimura T, Komagata K. Emendation of the genus Acidomonas Urakami, Tamaoka, Suzuki and Komagata 1989. Int J Syst Evol Microbiol 2004; 54: 865 870 [CrossRef] [PubMed]
    [Google Scholar]
  53. Greenberg DE, Porcella SF, Stock F, Wong A, Conville PS et al. Granulibacter bethesdensis gen. nov., sp. nov., a distinctive pathogenic acetic acid bacterium in the family Acetobacteraceae . Int J Syst Evol Microbiol 2006; 56: 2609 2616 [CrossRef] [PubMed]
    [Google Scholar]
  54. Lisdiyanti P, Kawasaki H, Widyastuti Y, Saono S, Seki T et al. Kozakia baliensis gen. nov., sp. nov., a novel acetic acid bacterium in the alpha-proteobacteria. Int J Syst Evol Microbiol 2002; 52: 813 818 [CrossRef] [PubMed]
    [Google Scholar]
  55. Yukphan P, Malimas T, Potacharoen W, Tanasupawat S, Tanticharoen M et al. Neoasaia chiangmaiensis gen. nov., sp. nov., a novel osmotolerant acetic acid bacterium in the alpha-Proteobacteria. J Gen Appl Microbiol 2005; 51: 301 311 [CrossRef] [PubMed]
    [Google Scholar]
  56. Jojima Y, Mihara Y, Suzuki S, Yokozeki K, Yamanaka S et al. Saccharibacter floricola gen. nov., sp. nov., a novel osmophilic acetic acid bacterium isolated from pollen. Int J Syst Evol Microbiol 2004; 54: 2263 2267 [CrossRef] [PubMed]
    [Google Scholar]
  57. Loganathan P, Nair S. Swaminathania salitolerans gen. nov., sp. nov., a salt-tolerant, nitrogen-fixing and phosphate-solubilizing bacterium from wild rice (Porteresia coarctata Tateoka). Int J Syst Evol Microbiol 2004; 54: 1185 1190 [CrossRef] [PubMed]
    [Google Scholar]
  58. Yukphan P, Malimas T, Muramatsu Y, Takahashi M, Kaneyasu M et al. Tanticharoenia sakaeratensis gen. nov., sp. nov., a new osmotolerant acetic acid bacterium in the α- Proteobacteria . Biosci Biotechnol Biochem 2008; 72: 672 676 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004666
Loading
/content/journal/ijsem/10.1099/ijsem.0.004666
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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