1887

Abstract

Strain EAR8 is a root endophyte isolated from plants collected from the Odiel marshes, Huelva (Spain). It presented plant growth-promoting properties and improved the plant growth and heavy metal accumulation in polluted soils playing an important role in phytoremediation strategies. Phenotypically, strain EAR8 cells were Gram-positive, aerobic and non-motile rods with terminal oval endospores and non-swollen sporangia which form beige, opaque, butyrous, raised and irregular colonies with undulate margins. The strain was able to grow between 15–45 °C, at pH 6.0–9.0 and tolerated 0–25 % NaCl (w/v) showing optimal growth conditions on trypticase soy agar plates supplemented with 2.5 % NaCl (w/v) at pH 7.0 and 37 °C for 24 h. Chemotaxonomic analyses showed that the isolate has -diaminopimelic acid as the peptidoglycan in the cell wall and MK-7 as the major respiratory quinone. The predominant fatty acids were anteiso-C and iso-C and the polar lipid profile was composed of diphosphatidylglycerol, phosphatidylglycerol and phosphatidylethanolamine. Phylogenetic analyses based on the whole proteomes of closest sequenced relatives confirmed that strain EAR8 is affiliated to the genus and forms a clade with 15-1 with maximum support. Genome analyses showed that EAR8 has indole-3-acetic acid and siderophore biosynthesis and transporters genes and genes related to resistance against heavy metals. Phenotypic and phylogenomic comparative studies suggested that strain EAR8 is a new representative of the genus and the name sp. nov. is proposed. Type strain is EAR8 (=CECT 9072=DSM 103900).

Funding
This study was supported by the:
  • universidad de salamanca (Award Postodoctoral fellowship)
    • Principle Award Recipient: LorenaCarro
  • inia (Award RTA 2012-0006-C03-03 project)
    • Principle Award Recipient: SalvadoraNavarro-Torre
  • junta de andalucía (Award P11-RNM-7274MO)
    • Principle Award Recipient: SalvadoraNavarro-Torre
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005015
2021-10-19
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/10/ijsem005015.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.005015&mimeType=html&fmt=ahah

References

  1. Gupta RS, Patel S, Saini N, Chen S. Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species. Int J Syst Evol Microbiol 2020; 70:5753–5798 [View Article] [PubMed]
    [Google Scholar]
  2. 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 [View Article] [PubMed]
    [Google Scholar]
  3. Yoon J-H, Kim I-G, Kang KH, T-K O, Park Y-H. Bacillus marisflavi sp. nov. and Bacillus aquimaris sp. nov., isolated from sea water of a tidal flat of the Yellow Sea in Korea. Int J Syst Evol Microbiol 2003; 53:1297–1303 [View Article] [PubMed]
    [Google Scholar]
  4. Noguchi H, Uchino M, Shida O, Takano K, Nakamura LK et al. Bacillus vietnamensis sp. nov., a moderately halotolerant, aerobic, endospore-forming bacterium isolated from Vietnamese fish sauce. Int J Syst Evol Microbiol 2004; 54:2117–2120 DOI: DOI: 10.1099/ijs.0.02895-0 [PubMed]
    [Google Scholar]
  5. Dastager SG, Mawlankar R, Tang SK, Srinivasan K, Ramana VV et al. Bacillus enclensis sp. nov., isolated from sediment sample. Antonie vanVan Leeuwenhoek 2014; 105:199–206 DOI: DOI: 10.1007/s10482-013-0066-3 [PubMed]
    [Google Scholar]
  6. Navarro-Torre S, Mateos-Naranjo E, Caviedes MA, Pajuelo E, Rodríguez-Llorente ID. Isolation of plant-growth-promoting and metal-resistant cultivable bacteria from Arthrocnemum macrostachyum in the Odiel marshes with potential use in phytoremediation. Mar Pollut Bull 110:133–142S0025-326X(16)30474-X [View Article] [PubMed]
    [Google Scholar]
  7. Navarro-Torre S, Barcia-Piedras JM, Caviedes MA, Pajuelo E, Redondo-Gómez S et al. Bioaugmentation with bacteria selected from the microbiome enhances Arthrocnemum macrostachyum metal accumulation and tolerance. Mar Pollut Bull 2017; 117:340–347 [View Article] [PubMed]
    [Google Scholar]
  8. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y. 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]
  9. Meier-Kolthoff JP, Göker M, Spröer C, Klenk H-P. When should a DDH experiment be mandatory in microbial taxonomy. Arch Microbiol 2013; 195:413–418 [View Article]
    [Google Scholar]
  10. 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]
  11. Montero-Calasanz MC, Göker M, Pötter G, Rohde M, Spröer C et al. Geodermatophilus arenarius sp. nov., a xerophilic actinomycete isolated from Saharan desert sand in Chad. Extremophiles 2012; 16:903–909 DOI: DOI: 10.1007/s00792-012-0486-4 [PubMed]
    [Google Scholar]
  12. Chun J, Oren A, Ventosa A, Christensen H, Ruiz Arahal D 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 DOI: DOI: 10.1099/ijsem.0.002516 [PubMed]
    [Google Scholar]
  13. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article] [PubMed]
    [Google Scholar]
  14. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM; 2013arXiv:1303.3997v2
  15. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  16. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  17. 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 DOI: DOI: 10.1186/1471-2164-9-75 [PubMed]
    [Google Scholar]
  18. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  19. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011; 8:785–786 [View Article] [PubMed]
    [Google Scholar]
  20. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001; 305:567–580 [View Article] [PubMed]
    [Google Scholar]
  21. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007; 35:W52–W57 [View Article] [PubMed]
    [Google Scholar]
  22. Krawczyk PS, Lipinski L, Dziembowski A. PlasFlow: predicting plasmid sequences in metagenomic data using genome signatures. Nucleic Acids Res 2018; 46:e35 [View Article] [PubMed]
    [Google Scholar]
  23. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
    [Google Scholar]
  24. Lefort V, Desper R, Gascuel O. FastME 2.0: A comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
    [Google Scholar]
  25. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–667 [View Article]
    [Google Scholar]
  26. Kreft L, Botzki A, Coppens F, Vandepoele K, Van Bel M. PhyD3: A phylogenetic tree viewer with extended phyloXML support for functional genomics data visualization. Bioinformatics 2017; 33:2946–2947 [View Article] [PubMed]
    [Google Scholar]
  27. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
    [Google Scholar]
  28. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article] [PubMed]
    [Google Scholar]
  29. Marathe R, Phatake Y, Sonawane A. Bioprospecting of Pseudomonas aeruginosa for their potential to produce siderophore: process optimization and evaluation of its bioactivity. Int J Bioassays 2015; 4:3667–3675
    [Google Scholar]
  30. Hotta K, Kim CY, Fox DT, Koppisch AT. Siderophore-mediated iron acquisition in Bacillus anthracis and related strains. Microbiology 2010; 156:1918–1925 [View Article] [PubMed]
    [Google Scholar]
  31. May JJ, Wendrich TM, Marahiel MA. The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 2001; 276:7209–7217 [View Article] [PubMed]
    [Google Scholar]
  32. Duca DR, Glick BR. Indole-3-acetic acid biosynthesis and its regulation in plant-associated bacteria. Appl Microbiol Biotechnol 2020; 104:8607–8619 [View Article]
    [Google Scholar]
  33. Perley JW, Stowe BB. On the ability of Taphrina deformans to produce indoleacetic acid from tryptophan by way of tryptamine. Plant Physiol 1966; 41:234–237 [View Article] [PubMed]
    [Google Scholar]
  34. Kato Y, Nakamura K, Sakiyama H, Mayhew SG, Asano Y. Novel heme-containing lyase, phenylacetaldoxime dehydratase from Bacillus sp. strain OxB-1: Purification, characterization, and molecular cloning of the gene. Biochemistry 2000; 39:800–809 [View Article] [PubMed]
    [Google Scholar]
  35. Bangash A, Iftikhar A, Saira A, Takuji K, Armghan S et al. Kushneria pakistanensis sp. nov., a novel moderately halophilic bacterium isolated from rhizosphere of a plant (Saccharum spontaneum) growing in salt mines of the Karak area in Pakistan. Antonie van Leeuwenhoek 2015; 107:991–1000 DOI: DOI: 10.1007/s10482-015-0391-9
    [Google Scholar]
  36. Zou Z, Wang G. Kushneria sinocarnis sp. nov., a moderately halophilic bacterium isolated from a Chinese traditional cured meat. Int J Syst Evol Microbiol 2010; 60:1881–1886 [View Article] [PubMed]
    [Google Scholar]
  37. Halebian S, Harris B, Finegold SM, Rolfe RD. Rapid method that aids in distinguishing Gram-positive from Gram-negative anaerobic bacteria. J Clin Microbiol 1981; 13:444–448 [View Article] [PubMed]
    [Google Scholar]
  38. Hong SW, Kwon SW, Kim SJ, Kim SY, Kim JJ et al. Bacillus oryzaecorticis sp. nov., a moderately halophilic bacterium isolated from rice husks. Int J Syst Evol Microbiol 2014; 64:2786–2791 DOI: DOI: 10.1099/ijs.0.058768-0 [PubMed]
    [Google Scholar]
  39. Logan NA, Vos PD. Bacillus. Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J. eds In Bergey’s Manual of Systematics of Archaea and Bacteria John Wiley & Sons, Inc., in association with Bergey’s Manual Trust; 2015 [View Article]
    [Google Scholar]
  40. Ventosa A, Nieto JJ, Oren A. Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 1998; 62:504–544 [View Article] [PubMed]
    [Google Scholar]
  41. Vaas LAI, Sikorski J, Michael V, Göker M, Klenk H-P. Visualization and curve parameter estimation strategies for efficient exploration of phenotype microarray kinetics. PLoS One 2012; 7:e34846 [View Article] [PubMed]
    [Google Scholar]
  42. Vaas LAI, Sikorski J, Hofner B, Fiebig A, Buddruhs N et al. opm: an R package for analyzing OmniLog (R) phenotype microarray data. Bioinformatics 2013; 29:1823–1824 DOI: DOI: 10.1093/bioinformatics/btt291 [PubMed]
    [Google Scholar]
  43. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athayle M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 DOI: DOI: 10.1016/0167-7012(84)90018-6
    [Google Scholar]
  44. Kroppenstedt RM, Goodfellow M. The family Thermonosporaceae: Actinocorallia, Actinomadura, Spirillispora y Thermomonospora. Dworkin M, Falkow S, Schleifer KH, Stackebrandt E. eds In Archaea y Bacteria, 3st ed. edn Vol 3 New York: Springer; 2006 pp 682–724
    [Google Scholar]
  45. Tindall BJ. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 1990; 13:128–130 [View Article]
    [Google Scholar]
  46. Tindall BJ. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 1990; 66:199–202 [View Article]
    [Google Scholar]
  47. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990; 20:16
    [Google Scholar]
  48. Staneck JL, Roberts GD. Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Microbiol 1974; 28:37 [View Article]
    [Google Scholar]
  49. Daroonpunt R, Yiamsombut S, Sitdhipol J, Tanasupawat S. Bacillus salacetis sp. nov., a slightly halophilic bacterium from Thai shrimp paste (Ka-pi). Int J Syst Evol Microbiol 2019; 69:1162–1168 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005015
Loading
/content/journal/ijsem/10.1099/ijsem.0.005015
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