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Volume 70, Issue 1

sp. nov., isolated from growing in the Odiel marshes(Spain) and emended descriptions of and Free

Abstract

Strain EAR18 was isolated as an endophyte from the roots of a halophyte plant, , growing in the Odiel marshes (Huelva, Spain). Cells of strain EAR18 were Gram- stain-negative, motile, non-spore-forming aerobic rods. It grew optimally on tryptic soy agar supplemented with 2.5 % NaCl (w/v), at pH 7 and 30 °C for 48 h. It tolerated NaCl from 0 to 25 % (w/v). It presented Q9 as the major quinone and C cyclo 8, summed feature 8 (Cω7 and/or Cω6) and C as the predominant fatty acids. The polar lipid profile consisted of diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine and four unidentified phospholipids. The results of phylogenetic analysis based on 16S rRNA gene sequences revealed that strain EAR18 formed a well-supported clade with species B6 and TRM 0175 (similarities of 98.3 and 96.1 % respectively). Furthermore, digital DNA–DNA hybridization analysis resulted in values of 20.4 % with TRM 0175 and 35.50 % with B6, and ANIb/ANIm results in values of 73.8 %/84.2 % with TRM 0175 and 86.8 %/89.4 % with B6. Based on phylogeny and differential phenotypic properties in comparison with its closest related species, strain EAR18 is suggested to represent a new species in the genus , for which the name sp. nov. is proposed. The type strain is EAR18 (=CECT 9077=LMG 29859). The whole genome was sequenced, and it had a total length of 4.6 Mbp and a G+C content of 64.9 mol%.

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  • Accepted:
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  • Published Online:
Keyword(s): endophyte , Halomonadaceae , heavy metals , PGPB and Plant growth-promoting bacteria
Funding
This study was supported by the:
  • Biotechnology and Biological Sciences Research Council (Award BB/L024209/1)
    • Principle Award Recipient: Not Applicable
  • Newcastle University (Award Postdoctoral fellow)
    • Principle Award Recipient: Lorena Carro
  • Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (Award RTA 2012-0006-C03-03)
    • Principle Award Recipient: Salvadora Navarro-Torre
  • Junta de Andalucía (Award P11-RNM-7274MO)
    • Principle Award Recipient: Salvadora Navarro-Torre
© 2020 The Authors
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2020-02-03
2024-05-12
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References

  1. Franzmann PD, Wehmeyer U, Stackebrandt E. Halomonadaceae fam. nov., a new family of the class Proteobacteria to accommodate the genera Halomonas and Deleya . Syst Appl Microbiol 1988; 11:16–19 [View Article]
     [Google Scholar]
  2. Dobson SJ, Franzmann PD. Unification of the genera Deleya (Baumann et al. 1983), Halomonas (Vreeland et al. 1980), and Halovibrio (Fendrich 1988) and the species Paracoccus halodenitrificans (Robinson and Gibbons 1952) into a single genus, Halomonas, and placement of the genus Zymobacter in the family Halomonadaceae . Int J Syst Bacteriol 1996; 46:550–558 [View Article]
     [Google Scholar]
  3. Ntougias S, Zervakis GI, Fasseas C. Halotalea alkalilenta gen. nov., sp. nov., a novel osmotolerant and alkalitolerant bacterium from alkaline olive mill wastes, and emended description of the family Halomonadaceae Franzmann et al. 1989, emend. Dobson and Franzmann 1996. Int J Syst Evol Microbiol 2007; 57:1975–1983 [View Article]
     [Google Scholar]
  4. Ben Ali Gam Z, Abdelkafi S, Casalot L, Thlozan L, Oueslati R et al. Modicisalibacter tunisiensis gen. nov., sp. nov., an aerobic, moderately halophilic bacterium isolated from an oilfield-water injection sample, and emended description of the family Halomonadaceae Franzmann, et al. 1989 emend Dobson and Franzmann 1996 emend. Ntougias, et al. 2007. Int J Syst Evol Microbiol 2007:2307–2313
     [Google Scholar]
  5. Vreeland RH, Litchfield CD, Martin EL, Elliot E, elongata H. Halomonas elongata, a new genus and species of extremely salt-tolerant bacteria. Int J Syst Bacteriol 1980; 30:485–495 [View Article]
     [Google Scholar]
  6. Parte AC. LPSN - List of Prokaryotic names with Standing in Nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 2018; 68:1825–1829 [View Article]
     [Google Scholar]
  7. Liu W, Zhang G, Xian W, Yang J, Yang L et al. Halomonas xiaochaidanensis sp. nov., isolated from a salt lake sediment. Arch Microbiol 2016; 198:761–766 [View Article]
     [Google Scholar]
  8. Zhang S, Pan J, Lu W, Yan Y, Wang H et al. Halomonas urumqiensis sp. nov., a moderately halophilic bacterium isolated from a saline-alkaline lake. Int J Syst Bacteriol 2016; 66:1962–1969
     [Google Scholar]
  9. Jung WY, Lee HJ, Jeon CO. Halomonas garicola sp. nov., isolated from saeu-jeot, a Korean salted and fermented shrimp sauce. Int J Syst Evol Microbiol 2016; 66:731–737 [View Article]
     [Google Scholar]
  10. Jiang W, Li C, Xu B, Dong X, Ma N et al. Halomonas shantousis sp. nov., a novel biogenic amines degrading bacterium isolated from Chinese fermented fish sauce. Antonie van Leeuwenhoek 2014; 106:1073–1080 [View Article]
     [Google Scholar]
  11. Lee J-C, Kim Y-S, Yun B-S, Whang K-S. Halomonas salicampi sp. nov., a halotolerant and alkalitolerant bacterium isolated from a saltern soil. Int J Syst Evol Microbiol 2015; 65:4792–4799 [View Article]
     [Google Scholar]
  12. Lee J-C, Kim S-J, Whang K-S. Halomonas sediminicola sp. nov., a moderately halophilic bacterium isolated from a solar saltern sediment. Int J Syst Evol Microbiol 2016; 66:3865–3872 [View Article]
     [Google Scholar]
  13. Dou G, He W, Liu H, Ma Y. Halomonas heilongjiangensis sp. nov., a novel moderately halophilic bacterium isolated from saline and alkaline soil. Antonie van Leeuwenhoek 2015; 108:403–413 [View Article]
     [Google Scholar]
  14. Wang Y-X, Xiao W, Dong M-H, Zhao Q, Li Z-Y et al. Halomonas qiaohouensis sp. nov., isolated from salt mine soil in southwest China. Antonie van Leeuwenhoek 2014; 106:253–260 [View Article]
     [Google Scholar]
  15. Gan L, Long X, Zhang H, Hou Y, Tian J et al. Halomonas saliphila sp. nov., a moderately halophilic bacterium isolated from a saline soil. Int J Syst Evol Microbiol 2018; 68:1153–1159 [View Article]
     [Google Scholar]
  16. Koh H-W, Rani S, Kim S-J, Moon E, Nam SW et al. Halomonas aestuarii sp. nov., a moderately halophilic bacterium isolated from a tidal flat. Int J Syst Evol Microbiol 2017; 67:4298–4303 [View Article]
     [Google Scholar]
  17. Gaboyer F, Vandenabeele-Trambouze O, Cao J, Ciobanu M-C, Jebbar M et al. Physiological features of Halomonas lionensis sp. nov., a novel bacterium isolated from a Mediterranean Sea sediment. Res Microbiol 2014; 165:490–500 [View Article]
     [Google Scholar]
  18. Kämpfer P, Rekha PD, Busse H-J, Arun AB, Priyanka P et al. Halomonas malpeensis sp. nov., isolated from rhizosphere sand of a coastal sand dune plant. Int J Syst Evol Microbiol 2018; 68:1037–1046 [View Article]
     [Google Scholar]
  19. Chen C, Anwar N, Wu C, Fu G, Wang R et al. Halomonas endophytica sp. nov., isolated from liquid in the stems of Populus euphratica . Int J Syst Evol Microbiol 2018; 68:1633–1638 [View Article]
     [Google Scholar]
  20. 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 2016; 110:133–142 [View Article]
     [Google Scholar]
  21. 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]
     [Google Scholar]
  22. Arahal DR, Vreeland RH, Litchfield CD, Mormile MR, Tindall BJ et al. Recommended minimal standards for describing new taxa of the family Halomonadaceae . Int J Syst Evol Microbiol 2007; 57:2436–2446 [View Article]
     [Google Scholar]
  23. Bangash A, Ahmed I, Abbas S, Kudo T, Shahzad A 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 [View Article]
     [Google Scholar]
  24. 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]
     [Google Scholar]
  25. 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
     [Google Scholar]
  26. 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]
     [Google Scholar]
  27. Vaas LAI, Sikorski J, Hofner B, Fiebig A, Buddruhs N et al. opm: an R package for analysing OmniLog(R) phenotype microarray data. Bioinformatics 2013; 29:1823–1824 [View Article]
     [Google Scholar]
  28. Minnikin DE, O'Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
     [Google Scholar]
  29. Kroppenstedt RM, Goodfellow M. The family Thermonosporaceae: Actinocorallia, Actinomadura, Spirillispora y Thermomonospora . In Dworkin M, Falkow S, Schleifer KH, Stackebrandt E et al. (editors) Archaea y Bacteria: Firmicutes, Actinomycetes: The Prokariotes 3, 3st ed. New York: Springer; 2006 pp 682–724
     [Google Scholar]
  30. 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]
  31. Tindall BJ. Lipid composition of Halobacterium lacusprofundi . FEMS Microbiol Lett 1990; 66:199–202 [View Article]
     [Google Scholar]
  32. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990; 20:16
     [Google Scholar]
  33. Yoon SH, SM H, 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
     [Google Scholar]
  34. Montero-Calasanz MdC, 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 [View Article]
     [Google Scholar]
  35. 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]
  36. 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]
  37. de la Haba RR, Márquez MC, Papke RT, Ventosa A. Multilocus sequence analysis of the family Halomonadaceae . Int J Syst Evol Microbiol 2012; 62:520–538 [View Article]
     [Google Scholar]
  38. 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]
  39. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
     [Google Scholar]
  40. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article]
     [Google Scholar]
  41. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM; 2013arXiv:1303.3997v2
  42. 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]
  43. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:7.5 [View Article]
     [Google Scholar]
  44. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article]
     [Google Scholar]
  45. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article]
     [Google Scholar]
  46. 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]
     [Google Scholar]
  47. 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]
     [Google Scholar]
  48. 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]
     [Google Scholar]
  49. 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]
     [Google Scholar]
  50. Guan T-W, Xiao J, Zhao K, Luo X-X, Zhang X-P et al. Halomonas xinjiangensis sp. nov., a halotolerant bacterium isolated from a salt lake. Int J Syst Evol Microbiol 2010; 60:349–352 [View Article]
     [Google Scholar]
  51. Xu L, Xu X-W, Meng F-X, Huo Y-Y, Oren A et al. Halomonas zincidurans sp. nov., a heavy-metal-tolerant bacterium isolated from the deep-sea environment. Int J Syst Evol Microbiol 2013; 63:4230–4236 [View Article]
     [Google Scholar]
  52. Ventosa A, Nieto JJ, Oren A. Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 1998; 62:504–544
     [Google Scholar]
  53. Vreeland RH. Halomonas. In Whitman B, Rainey F, Kämpfer P, Trujillo M, Chun J. (editors) In Bergey's manual of Systematics of Archaea and Bacteria 2015
     [Google Scholar]
  54. Tang X, Zhai L, Lin Y, Yao S, Wang L et al. Halomonas alkalicola sp. nov., isolated from a household product plant. Int J Syst Evol Microbiol 2017; 67:1546–1550 [View Article]
     [Google Scholar]
  55. 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]
     [Google Scholar]
  56. Mata JA, Martínez-Cánovas J, Quesada E, Béjar V. A detailed phenotypic characterisation of the type strains of Halomonas species. Syst Appl Microbiol 2002; 25:360–375 [View Article]
     [Google Scholar]
  57. Montero-Calasanz MdelC, Göker M, Rohde M, Spröer C, Schumann P et al. Chryseobacterium hispalense sp. nov., a plant-growth-promoting bacterium isolated from a rainwater pond in an olive plant nursery, and emended descriptions of Chryseobacterium defluvii, Chryseobacterium indologenes, Chryseobacterium wanjuense and Chryseobacterium gregarium . Int J Syst Evol Microbiol 2013; 63:4386–4395 [View Article]
     [Google Scholar]
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Halomonas radicis sp. nov., isolated from Arthrocnemum macrostachyum growing in the Odiel marshes(Spain) and emended descriptions of Halomonas xinjiangensis and Halomonas zincidurans
Int J Syst Evol Microbiol 70, 220 (2020); https://doi.org/10.1099/ijsem.0.003742
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