1887

Abstract

Strain MC02, a Gram-stain-negative, rod-shaped bacterium, was isolated from field soil collected from California, USA. To examine if MC02 represents a novel species, we compared its colony morphology, 16S rRNA gene and whole genome sequence, and its metabolic phenotype using Biolog GenIII and MALDI-TOF analyses compared to reference strains. Based on 16S rRNA gene and whole genome sequencing, MC02 belongs to the genus and K-3–1 is the most similar strain with 96.97 % 16S rRNA gene sequence identity. MALDI-TOF analysis revealed that DSM19289 is the closest match, but the similarity score was much lower than the ≥1.7 threshold for a reliable identification at the genus level. The predominant fatty acids were summed feature 3 (C⍵7 and/or C⍵6; 49.07 %) and C (30.01 %). The genome is 5.02 Mbp and the G+C content is 66.2 mol%. Whole genome comparisons to the closest related strains revealed an average amino acid identity value of 67.4 %, an OrthoANI similarity of 77.1 %, and a DNA–DNA-hybridization probability ≥70 %, confirming that MC02 represents a novel species. Strain MC02 can grow at pH 6 but not at pH 5, and a salt concentration of ≥1 % inhibits its growth. In contrast to other strains, MC02 can utilize turanose, inosine and -serine. The genome of MC02 shows putative endophyte genes such as a nitrate reductase, several phosphatases, and biotin biosynthesis genes, 26 flagellar motility genes and 14 invasion and intracellular resistance genes. Based on its metabolic, physiological and genomic characteristics, we propose that strain MC02 (NRRL B-65554=ATCC TSD-200=LMG 31737) represents a novel species of the genus with the name sp. nov.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004266
2020-06-08
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/70/6/3912.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004266&mimeType=html&fmt=ahah

References

  1. Egamberdieva D, Kamilova F, Validov S, Gafurova L, Kucharova Z et al. High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environ Microbiol 2008; 10:1–9
    [Google Scholar]
  2. Stewart EJ. Growing unculturable bacteria. J Bacteriol 2012; 194:4151–4160 [View Article]
    [Google Scholar]
  3. Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci 2012; 17:478–486 [View Article]
    [Google Scholar]
  4. Antoniou A, Tsolakidou M-D, Stringlis IA, Pantelides IS. Rhizosphere microbiome recruited from a suppressive compost improves plant fitness and increases protection against vascular wilt pathogens of tomato. Front Plant Sci 2017; 8: [View Article]
    [Google Scholar]
  5. Shi S, Nuccio E, Herman DJ, Rijkers R, Estera K et al. Successional trajectories of rhizosphere bacterial communities over consecutive seasons. MBio 2015; 6: [View Article]
    [Google Scholar]
  6. Garrity GM, Bell JA, Lilburn T. Bergey's Manual of Systematics of Archaea and Bacteria Bergey's Manual Trust; 2015
    [Google Scholar]
  7. La Scola B, Birtles RJ, Mallet Marie-Noëlle, Raoult D. Massilia timonae gen. nov., sp. nov., isolated from blood of an immunocompromised patient with cerebellar lesions. J Clin Microbiol 1998; 36:2847–2852 [View Article]
    [Google Scholar]
  8. Euzeby JP. List of prokaryotic names with standing in nomenclature. http://www.bacterio.net/ [accessed 2019].; 1997
  9. Xu P, Li W-J, Tang S-K, Zhang Y-Q, Chen G-Z et al. Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family ‘Oxalobacteraceae’ isolated from China. Int J Syst Evol Microbiol 2005; 55:1149–1153 [View Article]
    [Google Scholar]
  10. Kampfer P, Lodders N, Martin K, Falsen E. Revision of the genus Massilia La Scola, et al. 2000, with an emended description of the genus and inclusion of all species of the genus Naxibacter as new combinations, and proposal of Massilia consociata sp. nov.. Int J Syst Evol Microbiol 2011:61
    [Google Scholar]
  11. La Scola B, Birtles R, Mallet M, Raoult D. Massilia gen. nov. and Massilia timonae sp. nov. in list of new names and new combinations previously effectively, but not validly, published, validation list no. 73. Int J Syst Evol Microbiol 2000; 50:
    [Google Scholar]
  12. Chimwamurombe PM, Grönemeyer JL, Reinhold-Hurek B. Isolation and characterization of culturable seed-associated bacterial endophytes from gnotobiotically grown marama bean seedlings. FEMS Microbiol Ecol 2016; 92:11 [View Article]
    [Google Scholar]
  13. Ulrich K, Ulrich A, Ewald D. Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol Ecol 2008; 63:169–180 [View Article]
    [Google Scholar]
  14. JY L, Tian Z, JW Y, Yang M, Zhang Y. Distribution and abundance of antibiotic resistance genes in sand settling reservoirs and drinking water treatment plants across the yellow river, China. Water, Article 2018; 10:12
    [Google Scholar]
  15. Gallego V, Sánchez-Porro C, García MT, Ventosa A. Massilia aurea sp. nov., isolated from drinking water. Int J Syst Evol Microbiol 2006; 56:2449–2453 [View Article]
    [Google Scholar]
  16. Orthová I, Kämpfer P, Glaeser SP, Kaden R, Busse H-J. Massilia norwichensis sp. nov., isolated from an air sample. Int J Syst Evol Microbiol 2015; 65:56–64 [View Article]
    [Google Scholar]
  17. Guo B, Liu Y, Gu Z, Shen L, Liu K et al. Massilia psychrophila sp. nov., isolated from an ice core. Int J Syst Evol Microbiol 2016; 66:4088–4093 [View Article]
    [Google Scholar]
  18. Maya O, Yitzhak H, Dror M. Ecology of root colonizing Massilia (Oxalobacteraceae). PLoS One 2012; 7:
    [Google Scholar]
  19. Dohrmann AB, Tebbe CC. Effect of elevated tropospheric ozone on the structure of bacterial communities inhabiting the rhizosphere of herbaceous plants native to Germany. Appl Environ Microbiol 2005; 71:7750–7758 [View Article]
    [Google Scholar]
  20. Baldani JI, Rouws L, Cruz LM, Olivares FL, Schmid M et al. The Family Oxalobacteraceae. The Prokaryotes- Alphaproteobacteria and Betaproteobacteria Berlin Heidelberg: Springer-Verlag; 2014 pp 920–968
    [Google Scholar]
  21. Giuliano B, Gaspare C, Vincenzo A, Claudio DM, Francesca DF et al. Conventional farming impairs Rhizoctonia solani disease suppression by disrupting soil food web. J Phytopathol 2018; 166:663–673
    [Google Scholar]
  22. Agematu H, Suzuki K, Tsuya H, sp M. Massilia sp. BS-1, a novel violacein-producing bacterium isolated from soil. Biosci Biotechnol Biochem 2011; 75:2008–2010 [View Article]
    [Google Scholar]
  23. Hrynkiewicz K, Baum C, Leinweber P, Density LP. Density, metabolic activity, and identity of cultivable rhizosphere bacteria on Salix viminalis in disturbed arable and landfill soils. J Plant Nutr Soil Sci 2010; 173:747–756 [View Article]
    [Google Scholar]
  24. Ali N, Dashti N, Salamah S, Al-Awadhi H, Sorkhoh N et al. Autochthonous bioaugmentation with environmental samples rich in hydrocarbonoclastic bacteria for bench-scale bioremediation of oily seawater and desert soil. Environ Sci Pollut Res 2016; 23:8686–8698 [View Article]
    [Google Scholar]
  25. Abou-Shanab RAI, van Berkum P, Angle JS. Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale . Chemosphere 2007; 68:360–367 [View Article]
    [Google Scholar]
  26. Willgohs JA, Bleakley BH. Laboratory Manual for General Microbiology United States of America: Pearson; 2009
    [Google Scholar]
  27. 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]
    [Google Scholar]
  28. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article]
    [Google Scholar]
  29. Weon H-Y, Kim B-Y, Son J-A, Jang HB, Hong SK et al. Massilia aerilata sp. nov., isolated from an air sample. Int J Syst Evol Microbiol 2008; 58:1422–1425 [View Article]
    [Google Scholar]
  30. Rodríguez-Díaz M, Cerrone F, Sánchez-Peinado M, SantaCruz-Calvo L, Pozo C et al. Massilia umbonata sp. nov., able to accumulate poly-β-hydroxybutyrate, isolated from a sewage sludge compost–soil microcosm. Int J Syst Envol Microbiol 2014; 64:
    [Google Scholar]
  31. 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]
    [Google Scholar]
  32. Afgan E, Baker D, Batut B, van den Beek M, Bouvier D et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 2018; 46:W537–W544 [View Article]
    [Google Scholar]
  33. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article]
    [Google Scholar]
  34. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article]
    [Google Scholar]
  35. Kim M, Oh H-S, Park S-C, 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; 64:1825 [View Article]
    [Google Scholar]
  36. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015; 31:3210–3212 [View Article]
    [Google Scholar]
  37. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 2017; 45:D535–D542 [View Article]
    [Google Scholar]
  38. Overbeek R et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 2005; 33:5691–5702 [View Article]
    [Google Scholar]
  39. 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]
  40. Yoon S-H, Ha S-min, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article]
    [Google Scholar]
  41. 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 [View Article]
    [Google Scholar]
  42. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article]
    [Google Scholar]
  43. 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 [View Article]
    [Google Scholar]
  44. Auch AF, Klenk H-P, Göker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2010; 2:142–148 [View Article]
    [Google Scholar]
  45. Czaban J, Gajda A, Wroblewska B. The motility of bacteria from rhizosphere and different zones of winter wheat roots. Pol J Environ Stud 2007; 16:301–308
    [Google Scholar]
  46. BIOLOG Gen III MicroPlate instructions for use. Biolog Hayward, CA: Biolog; 2013
    [Google Scholar]
  47. Ihaka R, Gentleman R. R: a language for data analysis and graphics. J Comput Graph Stat 1996; 5:299–314
    [Google Scholar]
  48. Liu Y-Q, Wang B-J, Zhou N, Liu S-J. Undibacterium terreum sp. nov., isolated from permafrost soil. Int J Syst Evol Microbiol 2013; 63:2296–2300 [View Article]
    [Google Scholar]
  49. Sahin N, Portillo MC, Kato Y, Schumann P. Description of Oxalicibacterium horti sp. nov. and Oxalicibacterium faecigallinarum sp. nov., new aerobic, yellow-pigmented, oxalotrophic bacteria. FEMS Microbiol Lett 2009; 296:198–202 [View Article]
    [Google Scholar]
  50. Kämpfer P, P. Glaeser S, Lodders N, Busse H-J, Falsen E. Herminiimonas contaminans sp. nov., isolated as a contaminant of biopharmaceuticals. Int J Syst Evol Microbiol 2013; 63:412–417 [View Article]
    [Google Scholar]
  51. Pankiewicz KW, Goldstein BM. Inosine Monophosphate Dehydrogenase and Its Inhibitors: An Overview. Inosine Monophosphate Dehydrogenase Washington, DC: American Chemical Society;; 2003 pp 1–17
    [Google Scholar]
  52. Banerjee RV, Shane B, McGuire JJ, Coward JK. Dihydrofolate synthetase and folylpolyglutamate synthetase: direct evidence for intervention of acyl phosphate intermediates. Biochemistry 1988; 27:9062–9070 [View Article]
    [Google Scholar]
  53. Lincoln L, More SS. Bacterial invertases: occurrence, production, biochemical characterization, and significance of transfructosylation. J Basic Microbiol 2017; 57:803–813 [View Article]
    [Google Scholar]
  54. Zhao RL, Zhao R, YS T, Zhang XM, Deng LP et al. A novel alpha-galactosidase from the thermophilic probiotic Bacillus coagulans with remarkable protease-resistance and high hydrolytic activity. PLoS One 2018; 13:
    [Google Scholar]
  55. Sarkar P, Yarlagadda V, Ghosh C, Haldar J. A review on cell wall synthesis inhibitors with an emphasis on glycopeptide antibiotics. Medchemcomm 2017; 8:516–533 [View Article]
    [Google Scholar]
  56. Molodtsov V, Scharf NT, Stefan MA, Garcia GA, Murakami KS. Structural basis for rifamycin resistance of bacterial RNA polymerase by the three most clinically important RpoB mutations found in Mycobacterium tuberculosis . Mol Microbiol 2017; 103:1034–1045 [View Article]
    [Google Scholar]
  57. Chaudhary DK, Kim J. Massilia agri sp. nov., isolated from reclaimed grassland soil. Int J Syst Evol Microbiol 2017; 67:2696–2703 [View Article][PubMed]
    [Google Scholar]
  58. Zhao X, Li X, Qi N, Gan M, Pan Y et al. Massilia neuiana sp. nov., isolated from wet soil. Int J Syst Evol Microbiol 2017; 67:4943–4947 [View Article]
    [Google Scholar]
  59. Weon H-Y, Kim B-Y, Son J-A, Jang HB, Hong SK et al. Massilia aerilata sp. nov., isolated from an air sample. Int J Syst Evol Microbiol 2008; 58:1422–1425 [View Article]
    [Google Scholar]
  60. Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Front Microbiol 2015; 6: [View Article]
    [Google Scholar]
  61. Croxatto A, Prod'hom G, Greub G. Applications of MALDI-TOF mass spectrometry in clinical diagnostic microbiology. FEMS Microbiol Rev 2012; 36:380–407 [View Article]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.004266
Loading
/content/journal/ijsem/10.1099/ijsem.0.004266
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
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