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INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 71, Issue 5

sp. nov. and p. nov., two novel soil bacteria of the Free

Abstract

We isolated two new soil bacteria: ONC3 (from garden soil in NC, USA; LMG 31738=NRRL B-65553) and M1 (from farmed soil in MI, USA; NRRL B-65551=ATCC TSD-197=LMG 31739) and characterized their metabolic phenotype based on Biolog, MALDI-TOF MS and fatty acid analyses, and compared 16S rRNA and whole genome sequences to other members of the after sequencing on an Illumina Nextera platform. Based on the results of 16S rRNA sequence analysis, ONC3 shows the highest sequence similarity to J18 (97.8 %), J11 (97.7 %) and J9 (97.3 %). Strain M1 is most closely related to TSA40, K-1-15 and TSA66 (sequence identity of 98.2, 98.0 and 97.8 %, respectively). The whole genome of ONC3 has an assembled size of 5.62 Mbp, a G+C content of 63.8 mol% and contains 5104 protein-coding sequences, 56 tRNA genes and two rRNA operons. The genome of M1 has a length of 4.71 MBp, a G+C content of 63.81 mol% and includes 4967 protein-coding genes, two rRNA operons and 44 tRNA genes. Whole genome comparisons identified sp. WG5 with a 79.3 % average nucleotide identity (ANI) and 22.6 % digital DNA–DNA hybridization (dDDH), and sp. UBA11196 with 78.2 % average amino acid identity (AAI) as the most closely related species to ONC3. M1 is most closely related to TSA66 with an ANI of 80.27 %, or TSA40 with a dDDH of 22.3 %. The application of community-accepted standards such as <98.7 % in 16S sequence similarity and <95–96 % ANI or 70 % DDH support the classification of ONC3 and M1 as novel species within the .

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Massilia , Noviherbaspirillum , Oxalobacteraceae and plant-growth promoting rhizobacteria
Funding
This study was supported by the:
  • Agricultural Experiment Station, South Dakota State University
    • Principle Award Recipient: BückingHeike
  • Novozymes North America
    • Principle Award Recipient: BückingHeike
© 2021 The Authors
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2021-05-06
2024-05-07
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References

  1. Baldani JI, Rouws L, Cruz LM, Olivares FL, Schmid M. The family oxalobacteraceae. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. (editors) The Prokaryotes Berlin, Heidelberg: Springer Berlin Heidelberg; 2014 pp 919–974
     [Google Scholar]
  2. Ofek M, Hadar Y, Minz D. Ecology of root colonizing Massilia (Oxalobacteraceae). PLoS One 2012; 7:e40117 [View Article][PubMed]
     [Google Scholar]
  3. Pereira TP, do Amaral FP, Dall'Asta P, Brod FC, Arisi AC. Real-time PCR quantification of the plant growth promoting bacteria Herbaspirillum seropedicae strain SmR1 in maize roots. Mol Biotechnol 2014; 56:660–670 [View Article][PubMed]
     [Google Scholar]
  4. de Jesus Santos AF, Martins CYS, Santos PO, Corrêa Élida Barbosa, Barbosa HR et al. Diazotrophic bacteria associated with sisal (Agave sisalana Perrine ex Engelm): potential for plant growth promotion. Plant Soil 2014; 385:37–48 [View Article]
     [Google Scholar]
  5. Cerboneschi M, Decorosi F, Biancalani C, Ortenzi MV, Macconi S et al. Indole-3-acetic acid in plant-pathogen interactions: a key molecule for in planta bacterial virulence and fitness. Res Microbiol 2016; 167:774–787 [View Article][PubMed]
     [Google Scholar]
  6. Schlemper TR, Dimitrov MR, Silva Gutierrez FAO, van Veen JA, Silveira APD et al. Effect of Burkholderia tropica and Herbaspirillum frisingense strains on sorghum growth is plant genotype dependent. PeerJ 2018; 6:e5346 [View Article][PubMed]
     [Google Scholar]
  7. Feng GD, Yang SZ, Li H-P, Zhu H-H. Massilia putida sp. nov., a dimethyl disulfide-producing bacterium isolated from Wolfram mine tailing. Int J Syst Evol Microbiol 2016; 66:50–55 [View Article][PubMed]
     [Google Scholar]
  8. Zhang Y-Q, Li W-J, Zhang K-Y, Tian X-P, Jiang Y et al. Massilia dura sp. nov., Massilia albidiflava sp. nov., Massilia plicata sp. nov. and Massilia lutea sp. nov., isolated from soils in China. Int J Syst Evol Microbiol 2006; 56:459–463 [View Article][PubMed]
     [Google Scholar]
  9. La Scola B, Birtles RJ, Mallet MN, 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][PubMed]
     [Google Scholar]
  10. Sugiyama A, Ueda Y, Zushi T, Takase H, Yazaki K. Changes in the bacterial community of soybean rhizospheres during growth in the field. PLoS One 2014; 9:e100709 [View Article][PubMed]
     [Google Scholar]
  11. Zheng BX, Bi Q-F, Hao X-L, Zhou G-W, Yang X-R. Massilia phosphatilytica sp. nov., a phosphate solubilizing bacteria isolated from a long-term fertilized soil. Int J Syst Evol Microbiol 2017; 67:2514–2519 [View Article][PubMed]
     [Google Scholar]
  12. Kuffner M, De Maria S, Puschenreiter M, Fallmann K, Wieshammer G et al. Culturable bacteria from Zn- and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 2010; 108:1471–1484 [View Article][PubMed]
     [Google Scholar]
  13. Hrynkiewicz K, Baum C, Leinweber P. 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]
  14. Ishii S, Ashida N, Ohno H, Segawa T, Yabe S et al. Noviherbaspirillum denitrificans sp. nov., a denitrifying bacterium isolated from rice paddy soil and Noviherbaspirillum autotrophicum sp. nov., a denitrifying, facultatively autotrophic bacterium isolated from rice paddy soil and proposal to reclassify Herbaspirillum massiliense as Noviherbaspirillum massiliense comb. nov. Int J Syst Evol Microbiol 2017; 67:1841–1848 [View Article][PubMed]
     [Google Scholar]
  15. Chaudhary DK, Kim J. Noviherbaspirillum agri sp. nov., isolated from reclaimed grassland soil, and reclassification of Herbaspirillum massiliense (Lagier et al., 2014) as Noviherbaspirillum massiliense comb. nov. Int J Syst Evol Microbiol 2017; 67:1508–1515 [View Article][PubMed]
     [Google Scholar]
  16. Zhou X, Wang J-T, Zhang Z-F, Li W, Chen W et al. Microbiota in the rhizosphere and seed of rice from China, with reference to their transmission and biogeography. Front Microbiol 2020; 11:995 [View Article][PubMed]
     [Google Scholar]
  17. USDA 2019; Web Soil Survey [Internet]. https://websoilsurvey.sc.egov.usda.gov/
  18. California Soil Resource Lab 2019; USDA Natural Resources Conservation Service [Internet]. SoilWeb. https://casoilresource.lawr.ucdavis.edu/gmap/ cited December 08, 2019
  19. Soil Survey Staff NRCS 2017; United States Department of Agriculture. [Internet]. Web Soil Survey. https://websoilsurvey.sc.egov.usda.gov/ cited December 08, 2019
  20. Reasoner DJ, Geldreich EE. A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 1985; 49:1–7 [View Article][PubMed]
     [Google Scholar]
  21. Peta V, Raths R, Bücking H. Draft genome sequence of Massilia sp. strain ONC3, a novel bacterial species of the Oxalobacteraceae family isolated from garden soil. Microbiol Resour Announc 2019; 8:e00377–00319 [View Article][PubMed]
     [Google Scholar]
  22. Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A. Assembling genomes and mini-metagenomes from highly chimeric reads. Res Comput Mole Biol, Berlin, Heidelberg Springer Berlin Heidelberg 2013
     [Google Scholar]
  23. Simao 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][PubMed]
     [Google Scholar]
  24. 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]
  25. 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][PubMed]
     [Google Scholar]
  26. 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][PubMed]
     [Google Scholar]
  27. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:75 [View Article][PubMed]
     [Google Scholar]
  28. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article][PubMed]
     [Google Scholar]
  29. 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]
  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 [View Article][PubMed]
     [Google Scholar]
  31. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
     [Google Scholar]
  32. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article][PubMed]
     [Google Scholar]
  33. Jayaswal V, Robinson J, Jermiin L. Estimation of phylogeny and invariant sites under the general Markov model of nucleotide sequence evolution. Syst Biol 2007; 56:155–162 [View Article][PubMed]
     [Google Scholar]
  34. Letunic I, Bork P. Interactive tree of life (iTOL) V3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article][PubMed]
     [Google Scholar]
  35. Raina V, Nayak T, Ray L, Kumari K, Suar M. A polyphasic taxonomic approach for designation and description of novel microbial species. In Das S, Dash HR. (editors) Microbial Diversity in the Genomic Era 2019 pp 137–152
     [Google Scholar]
  36. Alanjary M, Steinke K, Ziemert N. AutoMLST: an automated web server for generating multi-locus species trees highlighting natural product potential. Nucleic Acids Res 2019; 47:W276–W282 [View Article][PubMed]
     [Google Scholar]
  37. Eddy SR. Profile hidden Markov models. Bioinformatics 1998; 14:755–763 [View Article][PubMed]
     [Google Scholar]
  38. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
     [Google Scholar]
  39. Rodriguez-R LM, Gunturu S, Harvey WT, Rossello-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. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007; 73:5261–5267 [View Article][PubMed]
     [Google Scholar]
  41. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2020; 36:1925–1927
     [Google Scholar]
  42. Arkin AP, Cottingham RW, Henry CS, Harris NL et al. KBase: The United States Department of Energy Systems Biology Knowledgebase; 2018; 36566
  43. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article][PubMed]
     [Google Scholar]
  44. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article][PubMed]
     [Google Scholar]
  45. Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
     [Google Scholar]
  46. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
     [Google Scholar]
  47. Auch AF, von Jan M, Klenk H-P, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2:117–134 [View Article][PubMed]
     [Google Scholar]
  48. Medlar AJ, Toronen 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]
  49. UniProt Consortium UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res 2019; 47:D506–D515 [View Article][PubMed]
     [Google Scholar]
  50. Bochner B. "Breathprints" at the microbial level. ASM News 1989; 55:536–539
     [Google Scholar]
  51. Venables WN, Ripley BD. Modern Applied Statistics with S, 4th ed. Springer; 2002
     [Google Scholar]
  52. Ihaka R, Gentleman R. Gentleman R. R: A language for data analysis and graphics. J Comput Graph Stat 1996; 5:299–314
     [Google Scholar]
  53. Raths R, Peta V, Bücking H. Massilia arenosa sp. nov., isolated from the soil of a cultivated maize field. Int J Syst Evol Microbiol 2020; 70:3912–3920 [View Article][PubMed]
     [Google Scholar]
  54. Bender RA. Regulation of the histidine utilization (hut) system in bacteria. Microbiol Mol Biol Rev 2012; 76:565–584 [View Article][PubMed]
     [Google Scholar]
  55. Schwede TF, Retey J, Schulz GE. Crystal structure of histidine ammonia-lyase revealing a novel polypeptide modification as the catalytic electrophile. Biochemistry 1999; 38:5355–5361 [View Article][PubMed]
     [Google Scholar]
  56. Cho J, Kim KH, Kim JO, Hong JS, Jeong SH et al. Massilia varians isolated from a clinical specimen. Infect Chemother 2017; 49:519–222 [View Article][PubMed]
     [Google Scholar]
  57. 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][PubMed]
     [Google Scholar]
  58. Choi SY, Yoon K-H, Lee JI, Mitchell RJ. Violacein: properties and production of a versatile bacterial pigment. Biomed Res Int 2015; 2015:1–8 [View Article][PubMed]
     [Google Scholar]
  59. Myeong NR, Seong HJ, Kim H-J, Sul WJ. Complete genome sequence of antibiotic and anticancer agent violacein producing Massilia sp. strain NR 4-1. J Biotechnol 2016; 223:36–37 [View Article][PubMed]
     [Google Scholar]
  60. 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][PubMed]
     [Google Scholar]
  61. Kong BH, Li YH, Liu M, Liu Y, Li CL et al. Massilia namucuonensis sp. nov., isolated from a soil sample. Int J Syst Evol Microbiol 2013; 63:352–357 [View Article][PubMed]
     [Google Scholar]
  62. Gallego V, Sánchez-Porro C, Garcia MT, Ventosa A. Massilia aurea sp. nov., isolated from drinking water. Int J Syst Evol Microbiol 2006; 56:2449–2453 [View Article][PubMed]
     [Google Scholar]
  63. Wilson BR, Bogdan AR, Miyazawa M, Hashimoto K, Tsuji Y. Siderophores in iron metabolism: from mechanism to therapy potential. Trends Mol Med 2016; 22:1077–1090 [View Article][PubMed]
     [Google Scholar]
  64. Ishige K, Zhang H, Kornberg A. Polyphosphate kinase (PPK2), a potent, polyphosphate-driven generator of GTP. Proc Natl Acad Sci U S A 2002; 99:16684–16688 [View Article][PubMed]
     [Google Scholar]
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Massilia horti sp. nov. and Noviherbaspirillum arenae sp. nov., two novel soil bacteria of the Oxalobacteraceae
Int J Syst Evol Microbiol 71, 004765 (2021); https://doi.org/10.1099/ijsem.0.004765
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