1887

Abstract

A novel strain was isolated from grassland soil that has the potential to assimilate ammonium by the reduction of nitrate in the presence of oxygen. Whole genome sequence analysis revealed the presence of an assimilatory cytoplasmic nitrate reductase gene and the assimilatory nitrite reductase genes which are involved in the sequential reduction of nitrate to nitrite and further to ammonium, respectively. Phylogenetic analysis based on 16S rRNA gene sequences revealed that the isolate represents a member of the genus . The closest phylogenetic neighbours based on 16S rRNA gene sequence analysis are the type strains of (98.17%) and (98.03%). In contrast, phylogenomic analysis revealed a close relationship to . Computation of the average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) with the closest phylogenetic neighbours of S1-A32-2 revealed genetic differences at the species level, which were further substantiated by differences in several physiological characteristics. On the basis of these results, it was concluded that the soil isolate represents a novel species of the genus for which the name sp. nov. (type strain S1-A32-2=LMG 31521=DSM 110222) is proposed.

Funding
This study was supported by the:
  • Deutsche Forschungsgemeinschaft (Award DFG Priority Program 1374)
    • Principle Award Recipient: SteffenKolb
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004799
2021-05-05
2024-04-25
Loading full text...

Full text loading...

References

  1. Peix A, Ramírez-Bahena M-H, Velázquez E. Historical evolution and current status of the taxonomy of genus Pseudomonas . Infect Genet Evol 2009; 9:1132–1147 [View Article][PubMed]
    [Google Scholar]
  2. Mulet M, Lalucat J, García-Valdés E. DNA sequence-based analysis of the Pseudomonas species. Environ Microbiol 2010; 12:1513–1530 [View Article][PubMed]
    [Google Scholar]
  3. García-Valdés E, Lalucat J. Pseudomonas: molecular phylogeny and current taxonomy. In Kahlon RS. editor Pseudomonas: Molecular and Applied Biology Cham: Springer International Publishing; 2016 pp 1–23
    [Google Scholar]
  4. Peix A, Ramírez-Bahena M-H, Velázquez E. The current status on the taxonomy of Pseudomonas revisited: an update. Infect Genet Evol 2018; 57:106–116 [View Article][PubMed]
    [Google Scholar]
  5. Palleroni NJ. Introduction to the family Pseudomonadaceae . In Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH. (editors) The Prokaryotes Berlin, New York, Heidelberg: Springer-Verlag; 1992 pp 3071–3085
    [Google Scholar]
  6. Silby MW, Winstanley C, Godfrey SAC, Levy SB, Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 2011; 35:652–680 [View Article][PubMed]
    [Google Scholar]
  7. Arai H. Regulation and function of versatile aerobic and anaerobic respiratory metabolism in Pseudomonas aeruginosa . Front Microbiol 2011; 2:103 [View Article][PubMed]
    [Google Scholar]
  8. Betlach MR, Tiedje JM, Firestone RB. Assimilatory nitrate uptake in Pseudomonas fluorescens studied using nitrogen-13. Arch Microbiol 1981; 129:135–140 [View Article][PubMed]
    [Google Scholar]
  9. Su W, Zhang L, Li D, Zhan G, Qian J et al. Dissimilatory nitrate reduction by Pseudomonas alcaliphila with an electrode as the sole electron donor. Biotechnol Bioeng 2012; 109:2904–2910 [View Article][PubMed]
    [Google Scholar]
  10. Pandey CB, Kumar U, Kaviraj M, Minick KJ, Mishra AK et al. DNRA: a short-circuit in biological N-cycling to conserve nitrogen in terrestrial ecosystems. Sci Total Environ 2020; 738:139710 [View Article][PubMed]
    [Google Scholar]
  11. Rütting T, Boeckx P, Müller C, Klemedtsson L. Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle. Biogeosciences 2011; 8:1779–1791 [View Article]
    [Google Scholar]
  12. Behrendt U, Schumann P, Stieglmeier M, Pukall R, Augustin J et al. Characterization of heterotrophic nitrifying bacteria with respiratory ammonification and denitrification activity – description of Paenibacillus uliginis sp. nov., an inhabitant of fen peat soil and Paenibacillus purispatii sp. nov., isolated from a spacecraft assembly clean room. Syst Appl Microbiol 2010; 33:328–336 [View Article][PubMed]
    [Google Scholar]
  13. Heylen K, Vanparys B, Wittebolle L, Verstraete W, Boon N et al. Cultivation of denitrifying bacteria: optimization of isolation conditions and diversity study. Appl Environ Microbiol 2006; 72:2637–2643 [View Article][PubMed]
    [Google Scholar]
  14. Behrendt U, Ulrich A, Schumann P. Fluorescent pseudomonads associated with the phyllosphere of grasses; Pseudomonas trivialis sp. nov., Pseudomonas poae sp. nov. and Pseudomonas congelans sp. nov. Int J Syst Evol Microbiol 2003; 53:1461–1469 [View Article][PubMed]
    [Google Scholar]
  15. 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]
  16. 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][PubMed]
    [Google Scholar]
  17. 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; 64:346–351 [View Article][PubMed]
    [Google Scholar]
  18. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article][PubMed]
    [Google Scholar]
  19. 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]
  20. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The seed and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:D206–D214 [View Article][PubMed]
    [Google Scholar]
  21. Lalucat J, Mulet M, Gomila M, García-Valdés E. Genomics in bacterial taxonomy: impact on the genus Pseudomonas . Genes 2020; 11:139 [View Article]
    [Google Scholar]
  22. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article][PubMed]
    [Google Scholar]
  23. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for bacteria and archaea. Nat Biotechnol 2020; 38:1079–1086 [View Article][PubMed]
    [Google Scholar]
  24. Behrendt U, Wende S, Kolb S, Ulrich A. Genome-based phylogeny of the genera Proteus and Cosenzaea and description of Proteus terrae subsp. terrae subsp. nov. and Proteus terrae subsp. cibarius subsp. nov. Int J Syst Evol Microbiol 2019; 71: 27 01 2021 [View Article][PubMed]
    [Google Scholar]
  25. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the bacteria and archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article][PubMed]
    [Google Scholar]
  26. Yoon S-H, Ha S-M, 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][PubMed]
    [Google Scholar]
  27. Varghese NJ, Mukherjee S, Ivanova N, Konstantinidis KT, Mavrommatis K et al. Microbial species delineation using whole genome sequences. Nucleic Acids Res 2015; 43:6761–6771 [View Article][PubMed]
    [Google Scholar]
  28. Palmer M, Steenkamp ET, Blom J, Hedlund BP, Venter SN. All ANIs are not created equal: implications for prokaryotic species boundaries and integration of ANIs into polyphasic taxonomy. Int J Syst Evol Microbiol 2020; 70:2937–2948 [View Article][PubMed]
    [Google Scholar]
  29. Palleroni NJ. Pseudomonas. In Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J. (editors) Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons, Ltd; 2015
    [Google Scholar]
  30. Meier-Kolthoff JP, Klenk H-P, Göker M. Taxonomic use of DNA G+C content and DNA–DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article][PubMed]
    [Google Scholar]
  31. Strejcek M, Smrhova T, Junkova P, Uhlik O. Whole-Cell MALDI-TOF MS versus 16S rRNA gene analysis for identification and Dereplication of recurrent bacterial isolates. Front Microbiol 2018; 9:1294 [View Article][PubMed]
    [Google Scholar]
  32. Müller T, Ruppel S, Behrendt U, Lentzsch P, Müller MEH. Antagonistic potential of fluorescent pseudomonads colonizing wheat heads against mycotoxin producing Alternaria and fusaria. Front Microbiol 2018; 9:2124 [View Article][PubMed]
    [Google Scholar]
  33. Behrendt U, Ulrich A, Schumann P, Erler W, Burghardt J et al. A taxonomic study of bacteria isolated from grasses: a proposed new species Pseudomonas graminis sp. nov. Int J Syst Bacteriol 1999; 49 Pt 1:297–308 [View Article][PubMed]
    [Google Scholar]
  34. Ryu E. On the Gram-differentiation of bacteria by the simplest method. J Jpn Soc Vet Sci 1938; 17:205–207 [View Article]
    [Google Scholar]
  35. Sun Y, De Vos P, Heylen K. Nitrous oxide emission by the non-denitrifying, nitrate ammonifier Bacillus licheniformis . BMC Genomics 2016; 17:68 [View Article][PubMed]
    [Google Scholar]
  36. Steinbüchel A, Oppermann-Sanio FB, Ewering C, Pötter M. Mikrobiologisches Praktikum Berlin, Heidelberg: Springer Spektrum; 2013
    [Google Scholar]
  37. Gadkari D. Influence of the herbicides Goltix and Sencor on nitrification process in two soils. Zentralbl Mikrobiol 1985; 140:547–554 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004799
Loading
/content/journal/ijsem/10.1099/ijsem.0.004799
Loading

Data & Media loading...

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