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Haloferax litoreum sp. nov., Haloferax marinisediminis sp. nov., and Haloferax marinum sp. nov., low salt-tolerant haloarchaea isolated from seawater and sediment

Abstract

Three novel halophilic archaea were isolated from seawater and sediment near Yeoungheungdo Island, Republic of Korea. The genome size and G + C content of the isolates MBLA0076T, MBLA0077T, and MBLA0078T were 3.56, 3.48, and 3.48 Mb and 61.7, 60.8, and 61.1 mol%, respectively. The three strains shared 98.5–99.5 % sequence similarity of the 16 S rRNA gene, whereas their sequence similarity to the 16 S rRNA gene of type strains was below 98.5 %. Phylogenetic analysis based on sequences of the 16 S rRNA and RNA polymerase subunit beta genes indicated that the isolates belonged to the genus Haloferax. The orthologous average nucleotide identity, average amino-acid identity, and in silico DNA-DNA hybridization values were below species delineation thresholds. Pan-genomic analysis indicated that the three novel strains and 11 reference strains had 8981 pan-orthologous groups in total. Fourteen Haloferax strains shared 1766 core pan-genome orthologous groups, which were mainly related to amino acid transport and metabolism. Cells of the three isolates were gram-negative, motile, red-pink pigmented, and pleomorphic. The strains grew optimally at 30 °C (MBLA0076T) and 40 °C (MBLA0077T, MBLA0078T) in the presence of 1.28 M (MBLA0077T) and 1.7 M (MBLA0076T, MBLA0078T) NaCl and 0.1 M (MBLA0077T), 0.2 M (MBLA0076T), and 0.3 M (MBLA0078T) MgCl2·6H2O at pH 7.0–8.0. Cells of all isolates lysed in distilled water; the minimum NaCl concentration necessary to prevent lysis was 0.43 M. The major polar lipids of the three strains were phosphatidylglycerol, phosphatidylglycerol phosphate methyl ester, and sulphated diglycosyl archaeol-1. Based on their phenotypic and genotypic properties, MBLA0076T, MBLA0077T, and MBLA0078T were described as novel species of Haloferax, for which we propose the names Haloferax litoreum sp. nov., Haloferax marinisediminis sp. nov., and Haloferax marinum sp. nov., respectively. The respective type strains of these species are MBLA0076T (= KCTC 4288T = JCM 34,169T), MBLA0077T (= KCTC 4289T = JCM 34,170T), and MBLA0078T (= KCTC 4290T = JCM 34,171T).

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Data availability

The GenBank/EMBL/DDBJ accession numbers for the genome sequences of strains MBLA0076T, MBLA0077T, and MBLA0078T are WKJO00000000, WKJP00000000 and WKJQ00000000, respectively. All data generated or analysed during this study are also included in this published article and its supplementary information files.

References

  1. Allen MA, Goh F, Leuko S, Echigo A, Mizuki T, Usami R, Kamekura M, Neilan BA, Burns BP (2008) Haloferax elongans sp. nov. and Haloferax mucosum sp. nov., isolated from microbial mats from Hamelin Pool, Shark Bay, Australia. Int J Syst Evol Microbiol 58:798–802. https://doi.org/10.1099/ijs.0.65360-0

    Article  PubMed  Google Scholar 

  2. Asgarani E, Funamizu H, Saito T, Terato H, Ohyama Y, Yamamoto O, Ide H (1999) Mechanisms of DNA protection in Halobacterium salinarium, an extremely halophilic bacterium. Microbiol Res 154:185–190. https://doi.org/10.1016/S0944-5013(99)80013-5

    Article  CAS  Google Scholar 

  3. Asker D, Ohta Y (2002) Haloferax alexandrinus sp. nov., an extremely halophilic canthaxanthin-producing archaeon from a solar saltern in Alexandria (Egypt). Int J Syst Evol Microbiol 52:729–738. https://doi.org/10.1099/00207713-52-3-729

    Article  PubMed  CAS  Google Scholar 

  4. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genome 9:75. https://doi.org/10.1186/1471-2164-9-75

    Article  CAS  Google Scholar 

  5. Bauer AW, Kirby MM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496. https://doi.org/10.1093/ajcp/45.4_ts.493

    Article  PubMed  CAS  Google Scholar 

  6. Benson HJ (2002) Microbiological Applications: Laboratory Manual in General Microbiology, 8th edn. McGraw-Hill, McGraw-Hill

    Google Scholar 

  7. Behera P, Mahapatra M, Seuylemezian A, Vaishampayan P, Ramana VV, Joseph N, Joshi A, Shouche Y, Suar M, Pattnaik AK, Rastogi G (2018) Taxonomic description and draft genome of Pseudomonas sediminis sp. nov., isolated from the rhizospheric sediment of Phragmites karka. J Microbiol 56:458–466. https://doi.org/10.1007/s12275-018-7549-x

    Article  PubMed  CAS  Google Scholar 

  8. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, Medema MH, Weber T (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucl Acids Res 47:W81–W87. https://doi.org/10.1093/nar/gkz310

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Bremer E, Krämer R (2019) Responses of microorganisms to osmotic stress. Annu Rev Microbiol 73:313–334. https://doi.org/10.1146/annurev-micro-020518-115504

    Article  PubMed  CAS  Google Scholar 

  10. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA III, Stevens R, Vonstein V, Wattam AR, Xia F (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365. https://doi.org/10.1038/srep08365

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Britton G, Liaaen-Jensen S, Pfander H (1995) Carotenoids, 1B: Spectroscopy. Birkhäuser, Basel

    Google Scholar 

  12. Burns DG, Janssen PH, Itoh T, Minegishi H, Usami R, Kamekura M, Dyall-Smith ML (2010) Natronomonas moolapensis sp. nov., non-alkaliphilic isolates recovered from a solar saltern crystallizer pond, and emended description of the genus Natronomonas. Int J Syst Evol Microbiol 60:1173–1176. https://doi.org/10.1099/ijs.0.010132-0

    Article  PubMed  CAS  Google Scholar 

  13. Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q (2005) VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33:D325–D328. https://doi.org/10.1093/nar/gki008

    Article  PubMed  CAS  Google Scholar 

  14. Chen S, He J, Zhang J, Xu Y, Huang J, Ke LX (2017) Halorubrum salsamenti sp. nov., a novel halophilic archaeon isolated from a brine of salt mine. Curr Microbiol 74:1358–1364. https://doi.org/10.1007/s00284-017-1325-8

    Article  PubMed  CAS  Google Scholar 

  15. Chen W, Hsu S-h, Lin M-T, Hsu Y-H (2015) Mass production of C50 carotenoids by Haloferax mediterranei in using extruded rice bran and starch under optimal conductivity of brined medium. Bioprocess Biosyst Eng 38:2361–2367. https://doi.org/10.1007/s00449-015-1471-y

    Article  PubMed  CAS  Google Scholar 

  16. Chaudhari NM, Gupta VK, Dutta C (2016) BPGA – an ultra-fast pan-genome analysis pipeline. Sci Rep 6:24373. https://doi.org/10.1038/srep24373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569. https://doi.org/10.1038/nmeth.2474

    Article  PubMed  CAS  Google Scholar 

  18. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466. https://doi.org/10.1099/ijsem.0.002516

    Article  PubMed  CAS  Google Scholar 

  19. den Besten HM, Mols M, Moezelaar R, Zwietering MH, Abee T (2009) Phenotypic and transcriptomic analyses of mildly and severely salt-stressed Bacillus cereus ATCC 14579 cells. Appl Environ Microbiol 75:4111–4119. https://doi.org/10.1128/AEM.02891-08

    Article  CAS  Google Scholar 

  20. D’Souza SE, Altekar W, D’Souza SF (1997) Adaptive response of Haloferax mediterranei to low concentrations of NaCl (< 20%) in the growth medium. Arch Microbiol 168:68–71. https://doi.org/10.1007/s002030050471

    Article  PubMed  Google Scholar 

  21. Dussault HP (1955) An improved technique for staining red halophilic bacteria. J Bacteriol 70:484–485

    Article  CAS  Google Scholar 

  22. Elshahed MS, Savage KN, Oren A, Gutierrez MC, Ventosa A, Krumholz LR (2004) Haloferax sulfurifontis sp. nov., a halophilic archaeon isolated from a sulfide- and sulfur-rich spring. Int J Syst Evol Microbiol 54:2275–2279. https://doi.org/10.1099/ijs.0.63211-0

    Article  PubMed  CAS  Google Scholar 

  23. Enache M, Itoh T, Kamekura M, Teodosiu G, Dumitru L (2007) Haloferax prahovense sp. nov. an extremely halophilic archaeon isolated from a Romanian salt lake. Int J Syst Evol Microbiol 57:393–397. https://doi.org/10.1099/ijs.0.64674-0

    Article  PubMed  CAS  Google Scholar 

  24. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359

    Article  PubMed  CAS  Google Scholar 

  25. Fang CJ, Ku KL, Lee MH, Su NW (2010) Influence of nutritive factors on C50 carotenoids production by Haloferax mediterranei ATCC 33500 with two-stage cultivation. Bioresour Technol 101:6487–6493. https://doi.org/10.1016/j.biortech.2010.03.044

    Article  PubMed  CAS  Google Scholar 

  26. Giani M, Martínez-Espinosa RM (2020) Carotenoids as a Protection Mechanism against Oxidative Stress in Haloferax mediterranei. Antioxidants 9:1060. https://doi.org/10.3390/antiox9111060

    Article  PubMed Central  CAS  Google Scholar 

  27. Gonzalez C, Gutierrez C, Ramirez C (1978) Halobacterium vallismortis sp. nov. an amylolytic and carbohydrate-metabolizing, extremely halophilic bacterium. Can J Microbiol 24:710–715. https://doi.org/10.1139/m78-119

    Article  PubMed  CAS  Google Scholar 

  28. Grant WD, Kamekura M, McGenity TJ, Ventosa A (2001) Class III. Halobacteria class. nov. In: Boone DR, Castenholz RW (eds) Bergey’s Manual of systematic bacteriology, vol 1, 2nd edn. The archaea and the deeply branching and phototrophic bacteria. Springer, New York, p 294

    Google Scholar 

  29. Gutierrez MC, Kamekura M, Holmes ML, Dyall-Smith ML, Ventosa A (2002) Taxonomic characterization of Haloferax sp. (‘‘H. alicantei’’) strain Aa 2.2: description of Haloferax lucentensis sp. nov. Extremophiles 6:479–483. https://doi.org/10.1007/s00792-002-0282-7

    Article  PubMed  CAS  Google Scholar 

  30. Gupta RS, Naushad S, Fabros R, Adeolu M (2016) A phylogenomic reappraisal of family-level divisions within the class Halobacteria: proposal to divide the order Halobacteriales into the families Halobacteriaceae, Haloarculaceae fam. nov., and Halococcaceae fam. nov., and the order Haloferacales into the families, Haloferacaceae and Halorubraceae fam nov. Antonie Van Leeuwenhoek 109:565–587. https://doi.org/10.1007/s10482-016-0660-2

    Article  PubMed  Google Scholar 

  31. Han D, Cui HL (2014) Haloplanus litoreus sp. nov. and Haloplanus ruber sp. nov., from a marine solar saltern and an aquaculture farm, respectively. Antonie Van Leeuwenhoek 105:679–685. https://doi.org/10.1007/s10482-014-0123-6

    Article  PubMed  CAS  Google Scholar 

  32. Horikoshi K, Antranikian G, Bull AT, Robb FT, Stetter KO (2011) Extremophiles handbook. Springer, Tokyo, p 608

    Book  Google Scholar 

  33. Holding A, Collee J (1971) Chapter I Routine biochemical tests. Methods Microbiol 6:1–32. https://doi.org/10.1016/S0580-9517(08)70573-7

    Article  Google Scholar 

  34. Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, Bork P (2017) Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Mol Biol Evol 34:2115–2122. https://doi.org/10.1093/molbev/msx148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Ismaeil M, Yoshida N, Katayama A (2018) Bacteroides sedimenti sp. nov., isolated from a chloroethenes-dechlorinating consortium enriched from river sediment. J Microbiol 56:619–627. https://doi.org/10.1007/s12275-018-8187-z

    Article  PubMed  CAS  Google Scholar 

  36. Juez G, Rodriguez-Valera F, Ventosa A, Kushner DJ (1986) Haloarcula hispanica spec. nov. and Haloferax gibbonsii spec. nov., two new species of extremely halophilic archaebacteria. Syst Appl Microbiol 8:75–79. https://doi.org/10.1016/S0723-2020(86)80152-7

    Article  Google Scholar 

  37. Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. https://doi.org/10.1093/nar/28.1.27

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066. https://doi.org/10.1093/nar/gkf436

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Kellermann MY, Yoshinaga MY, Valentine RC, Wörmer L, Valentine DL (2016) Important roles for membrane lipids in haloarchaeal bioenergetics. Biochim Biophys Acta 1858:2940–2956. https://doi.org/10.1016/j.bbamem.2016.08.010

    Article  PubMed  CAS  Google Scholar 

  40. Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of anurans. Syst Biol 18:1–32. https://doi.org/10.1093/sysbio/18.1.1

    Article  Google Scholar 

  41. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Kurt-Kızıldoğan A, Abanoz B, Okay S (2017) Global transcriptome analysis of Halolamina sp. to decipher the salt tolerance in extremely halophilic archaea. Gene 601:56–64. https://doi.org/10.1016/j.gene.2016.11.042

    Article  PubMed  CAS  Google Scholar 

  43. Lee I, Chalita M, Ha SM, Na SI, Yoon SH, Chun J (2017) ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int J Syst Evol Microbiol 67:2053–2057. https://doi.org/10.1099/ijsem.0.001872

    Article  PubMed  CAS  Google Scholar 

  44. Lee I, Kim YO, Park SC, Chun J (2015) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. https://doi.org/10.1099/ijsem.0.000760

    Article  PubMed  CAS  Google Scholar 

  45. Mandelli F, Miranda VS, Rodrigues E, Mercadante AZ (2012) Identification of carotenoids with high antioxidant capacity produced by extremophile microorganisms. World J Microbiol Biotechnol 28:1781–1790. https://doi.org/10.1007/s11274-011-0993-y

    Article  PubMed  CAS  Google Scholar 

  46. McDuff S, King GM, Neupane S, Myers MR (2016) Isolation and characterization of extremely halophilic CO-oxidizing Euryarchaeota from hypersaline cinders, sediments and soils and description of a novel CO oxidizer, Haloferax namakaokahaiae Mke2.3T, sp. nov. FEMS Microbiol Ecol 92:fiw028. https://doi.org/10.1093/femsec/fiw028

    Article  PubMed  CAS  Google Scholar 

  47. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60. https://doi.org/10.1186/1471-2105-14-60

    Article  Google Scholar 

  48. Medlar AJ, Toronen P, Holm L (2018) AAI-profiler: fast proteome-wide exploratory analysis reveals taxonomic identity, misclassification and contamination. Nucleic Acids Res 46:479–485. https://doi.org/10.1093/nar/gky359

    Article  CAS  Google Scholar 

  49. Minnikin DE, O’Donnell AG, Goodfellow M (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241. https://doi.org/10.1016/0167-7012(84)90018-6

    Article  CAS  Google Scholar 

  50. Montoro E, Lemus D, Echemendia M, Martin A, Portaels F, Palomino JC (2005) Comparative evaluation of the nitrate reduction assay, the MTT test, and the resazurin microtitre assay for drug susceptibility testing of clinical isolates of Mycobacterium tuberculosis. J Antimicrob Chemother 55:500–505. https://doi.org/10.1093/jac/dki023

    Article  PubMed  CAS  Google Scholar 

  51. Metris A, George SM, Mulholland F, Carter AT, Baranyi J (2014) Metabolic shift of Escherichia coli under salt stress in the presence of glycine betaine. Appl Environ Microbiol 80:4745–4756. https://doi.org/10.1128/AEM.00599-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Mullakhanbhai MF, Larsen H (1975) Halobacterium volcanii spec. nov., a Dead Sea halobacterium with a moderate salt requirement. Arch Microbiol 104:207–214. https://doi.org/10.1007/BF00447326

    Article  PubMed  CAS  Google Scholar 

  53. Oren A (2009) Microbial diversity and microbial abundance in salt-saturated brines: why are the waters of hypersaline lakes red? Natural Resources Environmental Issues 15:49

    Google Scholar 

  54. Oren A (2012) Taxonomy of the family Halobacteriaceae: a paradigm for changing concepts in prokaryote systematics. Int J Syst Evol Microbiol 62:263–271. https://doi.org/10.1099/ijs.0.038653-0

    Article  PubMed  Google Scholar 

  55. Oren A, Ventosa A, Grant W (1997) Proposed minimal standards for description of new taxa in the order Halobacteriales. Int J Syst Evol Microbiol 47:233–238. https://doi.org/10.1099/00207713-47-1-233

    Article  Google Scholar 

  56. Rodriguez-Valera F, Juez G, Kushner DJ (1983) Halobacterium mediterranei spec. nov., a new carbohydrate-utilizing extreme halophile. Syst Appl Microbiol 4:369–381. https://doi.org/10.1016/S0723-2020(83)80021-6

    Article  PubMed  CAS  Google Scholar 

  57. Saralov AI, Baslerov RV, Kuznetsov BB (2013) Haloferax chudinovii sp. nov., a halophilic archaeon from Permian potassium salt deposits. Extremophiles 17:499–504. https://doi.org/10.1007/s00792-013-0534-8

    Article  PubMed  CAS  Google Scholar 

  58. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  PubMed  CAS  Google Scholar 

  59. Shahmohammadi HR, Asgarani E, Terato H, Saito T, Ohyama Y, Gekko K, Yamamoto O, Ide H (1998) Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinarium against DNA-damaging agents. J Radiat Res 39:251–262. https://doi.org/10.1269/jrr.39.251

    Article  PubMed  CAS  Google Scholar 

  60. Sneath PH, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. Freeman, San Francisco

    Google Scholar 

  61. Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36. https://doi.org/10.1093/nar/28.1.33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Thombre RS, Shinde VD, Oke RS, Dhar SK, Shouche YS (2016) Biology and survival of extremely halophilic archaeon Haloarcula marismortui RR12 isolated from Mumbai salterns, India in response to salinity stress. Sci Rep 6:25642. https://doi.org/10.1038/srep25642

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Tittsler RP, Sandholzer LA (1936) The use of semi-solid agar for the detection of bacterial motility. J Bacteriol 31:575–580

    Article  CAS  Google Scholar 

  65. Tomlinson GA, Jahnke LL, Hochstein LI (1986) Halobacterium denitrificans sp. nov., an extremely halophilic denitrifying bacterium. Int J Syst Bacteriol 36:66–70. https://doi.org/10.1099/00207713-36-1-66

    Article  PubMed  CAS  Google Scholar 

  66. Torreblanca M, Rodriguez-Valera F, Juez G, Ventosa A, Kamekura M, Kates M (1986) Classification of non-alkaliphilic halobacteria based on numerical taxonomy and polar lipid composition, and description of Haloarcula gen. nov. and Haloferax gen. nov. Syst Appl Microbiol 8:89–99. https://doi.org/10.1016/S0723-2020(86)80155-2

    Article  Google Scholar 

  67. Vauclare P, Natali F, Kleman JP, Zaccai G, Franzetti B (2020) Surviving salt fluctuations: stress and recovery in Halobacterium salinarum, an extreme halophilic Archaeon. Sci Rep 10:1–10. https://doi.org/10.1038/s41598-020-59681-1

    Article  CAS  Google Scholar 

  68. Xu X-W, Wu Y-H, Wang C-S, Oren A, Zhou P-J, Wu M (2007) Haloferax larsenii sp. nov., an extremely halophilic archaeon from a solar saltern. Int J Syst Evol Microbiol 57:717–720. https://doi.org/10.1099/ijs.0.64573-0

    Article  PubMed  CAS  Google Scholar 

  69. Yang Y, Yatsunami R, Ando A, Miyoko N, Fukui T, Takaichi S, Nakamura S (2015) Complete biosynthetic pathway of the C50 carotenoid bacterioruberin from lycopene in the extremely halophilic archaeon Haloarcula japonica. J Bacteriol 197:1614–1623. https://doi.org/10.1128/JB.02523-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Yatsunami R, Ando A, Yang Y, Takaichi S, Kohno M, Matsumura Y, Ikeda H, Fukui T, Nakasone K, Fujita N, Sekine M, Takashina T, Nakamura S (2014) Identification of carotenoids from the extremely halophilic archaeon Haloarcula japonica. Front Microbiol 5:100. https://doi.org/10.3389/fmicb.2014.00100

    Article  PubMed  PubMed Central  Google Scholar 

  71. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Zhao Y, Wu J, Yang J, Sun S, Xiao J, Yu J (2012) PGAP: pan-genomes analysis pipeline. Bioinformatics 28:416–418. https://doi.org/10.1093/bioinformatics/btr655

    Article  PubMed  CAS  Google Scholar 

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Funding

This work was supported by an Incheon National University Research Grant in 2018.

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E-SC performed all the experiments and drafted the manuscript. I-TC and SWR contributed to isolate the strains and analyze the data. M-JS designed all the experiments and supervised the manuscript.

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Correspondence to Myung-Ji Seo.

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Cho, ES., Cha, IT., Roh, S.W. et al. Haloferax litoreum sp. nov., Haloferax marinisediminis sp. nov., and Haloferax marinum sp. nov., low salt-tolerant haloarchaea isolated from seawater and sediment. Antonie van Leeuwenhoek (2021). https://doi.org/10.1007/s10482-021-01661-0

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Keywords

  • Haloarchaea
  • Haloferax
  • Isolation
  • Low salt tolerance
  • Polyphasic taxonomy