1887

Abstract

A novel micro-organism designated AS10 was isolated from dry salt collected from Aveiro saltern in the north of Portugal. Cells were Gram-stain-positive, non-motile, non-endospore-forming, rod-shaped and aerobic. Strain AS10 was characterized by long filaments of rod-shaped cells, presenting also coccoid cellular forms at the end of the filaments, unveiling some pleomorphism. Rod-shaped cells varied from 0.3 to 0.6 µm wide and from 0.6 to 2 µm long. Growth of AS10 occurred at 15–40 °C (optimum, 20–30 °C), 0–10% (w/v) NaCl (optimum, 2%) and pH 4.5–11.0 (optimum, pH 8.0–11.0). The peptidoglycan type was A1ϒ-type with 3-hydroxy-diaminopimelic acid. The major fatty acids were C, iso-C, C and C. The major respiratory quinone was MK-9(H). Phylogenetic analysis based on 16S rRNA gene sequences showed that strain AS10 was similar to actinobacterial members of the class , with ANL-iso2 being the closest relative the species with a sequence pairwise similarity of 91.21%. Average nucleotide identity, average amino acid identity and DNA–DNA hybridization values between strain AS10 and ANL-iso2 were 71.34, 53.57 and 18.90%, respectively. The genome DNA G+C content of AS10 was 71.8 mol%. Based on genomic, phylogenetic, phenotypic and chemotaxonomic studies, we describe a new species of a novel genus represented by strain AS10 (=LMG 31937=CECT 30148) for which we propose the name gen. nov., sp. nov. We also propose that this organism represents a new family named fam. nov. of a novel order named ord. nov.

Funding
This study was supported by the:
  • Fundação para a Ciência e a Tecnologia (Award UIDB/04539/2020)
    • Principle Award Recipient: LucianaAlbuquerque
  • Fundação para a Ciência e a Tecnologia (Award NORTE-01-0145-FEDER-000035)
    • Principle Award Recipient: NotApplicable
  • Fundação para a Ciência e a Tecnologia (Award SFRH/BD/125527/2016)
    • Principle Award Recipient: EduardaAlmeida
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2022-02-09
2024-12-03
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References

  1. Almeida E, Henriques V, Wiegand S, Albuquerque L, Schumann P et al. Salsipaludibacter albus gen. nov., sp. nov., a novel actinobacterial strain isolate from a portuguese solar saltern and proposal of salsipaludibacteraceae fam. nov. and salsipaludibacterales ord. nov. Figshare 2021. DOI: 10.6084/m9.figshare.17102372.v1
    [Google Scholar]
  2. Zhang J, Ma G, Deng Y, Dong J, Van Stappen G et al. Bacterial diversity in bohai bay solar saltworks, China. Curr Microbiol 2016; 72:55–63 [View Article]
    [Google Scholar]
  3. Stackebrandt E, Rainey FA, Ward-rainey NL. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol 1997; 47:479–491 [View Article]
    [Google Scholar]
  4. Goodfellow M. Phylum XXVI. Actinobacteria phyl. nov. In Bergey’s Manual of Systematic Bacteriology Volume 5: The Actinobacteria 2012 pp 843–888
    [Google Scholar]
  5. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T et al. Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 2018; 9:1–119 [View Article]
    [Google Scholar]
  6. Ludwig W, Euzéby J, Schumann P, Busse H-J, Trujillo ME et al. Road map of the phylum Actinobacteria. In: Bergey’s Manual of Systematic Bacteriology Volume 5: The Actinobacteria 2012 pp 1–28
    [Google Scholar]
  7. Sorokin DY, van Pelt S, Tourova TP, Evtushenko LI. Nitriliruptor alkaliphilus gen. nov., sp. nov., a deep-lineage haloalkaliphilic actinobacterium from soda lakes capable of growth on aliphatic nitriles, and proposal of Nitriliruptoraceae fam. nov. and Nitriliruptorales ord. nov. Int J Syst Evol Microbiol 2009; 59:248–253 [View Article]
    [Google Scholar]
  8. Kurahashi M, Fukunaga Y, Sakiyama Y, Harayama S, Yokota A. Euzebya tangerina gen. nov., sp. nov., a deeply branching marine actinobacterium isolated from the sea cucumber Holothuria edulis, and proposal of Euzebyaceae fam. nov., Euzebyales ord. nov. and Nitriliruptoridae subclassis nov. Int J Syst Evol Microbiol 2010; 60:2314–2319 [View Article] [PubMed]
    [Google Scholar]
  9. Zhang Y-G, Chen J-Y, Wang H-F, Xiao M, Yang L-L et al. Egicoccus halophilus gen. nov., sp. nov., a halophilic, alkalitolerant actinobacterium and proposal of Egicoccaceae fam. nov. and Egicoccales ord. nov. Int J Syst Evol Microbiol 2016; 66:530–535 [View Article]
    [Google Scholar]
  10. Zhang Y-G, Wang H-F, Yang L-L, Zhou X-K, Zhi X-Y et al. Egibacter rhizosphaerae gen. nov., sp. nov., an obligately halophilic, facultatively alkaliphilic actinobacterium and proposal of Egibaceraceae fam. nov. and Egibacterales ord. nov. Int J Syst Evol Microbiol 2016; 66:283–289 [View Article]
    [Google Scholar]
  11. Lage OM, Bondoso J. Planctomycetes diversity associated with macroalgae. FEMS Microbiol Ecol 2011; 78:366–375 [View Article] [PubMed]
    [Google Scholar]
  12. Almeida E, Dias TV, Ferraz G, Carvalho MF, Lage OM. Culturable bacteria from two Portuguese salterns: diversity and bioactive potential. Antonie van Leeuwenhoek 2020; 113:459–475 [View Article] [PubMed]
    [Google Scholar]
  13. Staley JT. Prosthecomicrobium and Ancalomicrobium: new prosthecate freshwater bacteria. J Bacteriol 1968; 95:1921–1942 [View Article] [PubMed]
    [Google Scholar]
  14. Cohen-bazire G, Sistrom WR, Stanier RY. Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Comp Physiol 1957; 49:25–68 [View Article] [PubMed]
    [Google Scholar]
  15. Bondoso J, Albuquerque L, Nobre MF, Lobo-da-Cunha A, da Costa MS et al. Aquisphaera giovannonii gen. nov., sp. nov., a planctomycete isolated from a freshwater aquarium. Int J Syst Evol Microbiol 2011; 61:2844–2850 [View Article]
    [Google Scholar]
  16. Kuester E, Williams ST. Selection of media for isolation of streptomycetes. Nature 1964; 202:928–929 [View Article] [PubMed]
    [Google Scholar]
  17. Jensen PR, Gontang E, Mafnas C, Mincer TJ, Fenical W. Culturable marine actinomycete diversity from tropical Pacific Ocean sediments. Environ Microbiol 2005; 7:1039–1048 [View Article] [PubMed]
    [Google Scholar]
  18. Mincer TJ, Jensen PR, Kauffman CA, Fenical W. Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 2002; 68:5005–5011 [View Article] [PubMed]
    [Google Scholar]
  19. Webster NS, Wilson KJ, Blackall LL, Hill RT. Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 2001; 67:434–444 [View Article] [PubMed]
    [Google Scholar]
  20. Vickers JC, Williams ST, Ross GW. A taxonomic approach to selective isolation of Streptomycetes from soil. In Ortiz-Ortiz L, Bojalil LF, Yakoleff V. eds Biological, Biochemical, and Biomedical Aspects of Actinomycetes Orlando, Florida: Academic Press, Inc. (London) Ltd; 1984 pp 553–561
    [Google Scholar]
  21. Tindall BJ, Sikorski J, Smibert RA, Krieg NR et al. Phenotypic characterization and the principles of comparative systematics. In Reddy CA, Beveridge TJ, Breznak JA, Marzluf G, Schmidt TM. eds Methods for General and Molecular Microbiology, 3rd edn. Washington, DC: American Society of Microbiology; 2007 pp 330–393
    [Google Scholar]
  22. Harrison PJ, Waters RE, Taylor FJR. A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. J Phycol 1980; 16:28–35 [View Article]
    [Google Scholar]
  23. Xu P, Li W-J, Tang S-K, Zhang Y-Q, Chen G-Z et al. Naxibacter alkalitolerans gen. nov., sp. nov., a novel member of the family ‘Oxalobacteraceae’ isolated from China. Int J Syst Evol Microbiol 2005; 55:1149–1153 [View Article]
    [Google Scholar]
  24. Bondoso J, Albuquerque L, Lobo-da-Cunha A, da Costa MS, Harder J et al. Rhodopirellula lusitana sp. nov. and Rhodopirellula rubra sp. nov., isolated from the surface of macroalgae. Syst Appl Microbiol 2014; 37:157–164 [View Article] [PubMed]
    [Google Scholar]
  25. Christensen WB. Urea decomposition as a means of differentiating proteus and paracolon cultures from each other and from Salmonella and Shigella types. J Bacteriol 1946; 52:461–466 [View Article] [PubMed]
    [Google Scholar]
  26. Sierra G. A simple method for the detection of lipolytic activity of micro-organisms and some observations on the influence of the contact between cells and fatty substrates. Antonie van Leeuwenhoek 1957; 23:15–22 [View Article] [PubMed]
    [Google Scholar]
  27. Medina P, Baresi L. Rapid identification of gelatin and casein hydrolysis using TCA. J Microbiol Methods 2007; 69:391–393 [View Article] [PubMed]
    [Google Scholar]
  28. Cappuccino JG, Welsh C. Microbiology, A Laboratory Manual Pearson Education Limited; 2017 p 561
    [Google Scholar]
  29. Teather RM, Wood PJ. Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 1982; 43:777–780 [View Article] [PubMed]
    [Google Scholar]
  30. Schumann P. Peptidoglycan structure. In Methods in Microbiology Elsevier Ltd; 2011 pp 101–129
    [Google Scholar]
  31. de Costa MS, Albuquerque L, Nobre MF, Wait R. The identification of polar lipids in prokaryotes. In Rainey F, Oren A. eds Methods in Microbiology (Taxonomy of Prokaryotes) London, UK: Elsevier Ltd; 2011 pp 165–181
    [Google Scholar]
  32. de Costa MS, Albuquerque L, Nobre MF, Wait R. The extraction and identification of respiratory lipoquinones of prokaryotes and their use in taxonomy. In Rainey F, Oren A. eds Methods in Microbiology (Taxonomy of Prokaryotes) London, UK: Elsevier Ltd; 2011 pp 197–206
    [Google Scholar]
  33. de Costa MS, Albuquerque L, Nobre M, Wait R. The identification of fatty acids in Bacteria. In Rainey F, Oren A. eds Methods in Microbiology London, UK: Elsevier Ltd; 2011 pp 183–196
    [Google Scholar]
  34. 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]
  35. 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]
  36. 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]
  37. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  38. Wingett S. FastQ Screen - Contamination screening for NGS datasets UK: Babraham Institute; 2011 http://www.bioinformatics.babraham.ac.uk/projects/fastq_screen/fastq_screen_documentation.html
  39. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 2011; 27:863–864 [View Article] [PubMed]
    [Google Scholar]
  40. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011; 27:2957–2963 [View Article] [PubMed]
    [Google Scholar]
  41. 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] [PubMed]
    [Google Scholar]
  42. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011; 27:578–579 [View Article] [PubMed]
    [Google Scholar]
  43. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  44. 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]
  45. 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]
  46. 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]
  47. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ 2016; 4:e1900v1
    [Google Scholar]
  48. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article] [PubMed]
    [Google Scholar]
  49. Zhang H, Yohe T, Huang L, Entwistle S, Wu P et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 2018; 46:W95–W101 [View Article] [PubMed]
    [Google Scholar]
  50. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H et al. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 1999; 27:29–34 [View Article] [PubMed]
    [Google Scholar]
  51. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res 2011; 39:W347–52 [View Article] [PubMed]
    [Google Scholar]
  52. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 2006; 34:D32–6 [View Article] [PubMed]
    [Google Scholar]
  53. Bertelli C, Laird MR, Williams KP. Simon Fraser University Research Computing Group Lau BY et al. IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res 2017; 45:W30–W35 [View Article] [PubMed]
    [Google Scholar]
  54. Couvin D, Bernheim A, Toffano-Nioche C, Touchon M, Michalik J et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res 2018; 46:W246–W251 [View Article] [PubMed]
    [Google Scholar]
  55. Blin K, Shaw S, Steinke K, Villebro R, Ziemert N et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 2019; 47:W81–W87 [View Article] [PubMed]
    [Google Scholar]
  56. van Heel AJ, de Jong A, Song C, Viel JH, Kok J et al. BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res 2018; 46:W278–W281 [View Article] [PubMed]
    [Google Scholar]
  57. Ziemert N, Podell S, Penn K, Badger JH, Allen E et al. The natural product domain seeker NaPDoS: a phylogeny based bioinformatic tool to classify secondary metabolite gene diversity. PLoS One 2012; 7:e34064 [View Article] [PubMed]
    [Google Scholar]
  58. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
    [Google Scholar]
  59. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL. GenBank. Nucleic Acids Res 2005; 33:D34–8 [View Article]
    [Google Scholar]
  60. Yin Q, Zhang L, Song Z-M, Wu Y, Hu Z-L et al. Euzebya rosea sp. nov., a rare actinobacterium isolated from the East China Sea and analysis of two genome sequences in the genus Euzebya. Int J Syst Evol Microbiol 2018; 68:2900–2905 [View Article] [PubMed]
    [Google Scholar]
  61. Jian S-L, Xu L, Meng F-X, Sun C, Xu X-W. Euzebya pacifica sp. nov., a novel member of the class Nitriliruptoria. Int J Syst Evol Microbiol 2021; 71:004864 [View Article]
    [Google Scholar]
  62. Trujillo ME, Hong K, Genilloud O. The family Micromonosporaceae. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. eds The Prokaryotes Berlin, Heidelberg: Springer; 2014 pp 499–569
    [Google Scholar]
  63. Jostensen JP, Landfald B. Influence of growth conditions on fatty acid composition of a polyunsaturated-fatty-acid-producing Vibrio species. Arch Microbiol 1996; 165:306–310 [View Article] [PubMed]
    [Google Scholar]
  64. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article] [PubMed]
    [Google Scholar]
  65. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci USA 2005; 102:2567–2572 [View Article] [PubMed]
    [Google Scholar]
  66. Konstantinidis KT, Tiedje JM. Towards a genome-based taxonomy for prokaryotes. J Bacteriol 2005; 187:6258–6264 [View Article] [PubMed]
    [Google Scholar]
  67. Luo C, Rodriguez-R LM, Konstantinidis KT. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 2014; 42:e73 [View Article] [PubMed]
    [Google Scholar]
  68. Jordan IK, Rogozin IB, Wolf YI, Koonin EV. Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Res 2002; 12:962–968 [View Article] [PubMed]
    [Google Scholar]
  69. Pereira PN, Cushman JC. Exploring the relationship between crassulacean acid metabolism (CAM) and mineral nutrition with a special focus on nitrogen. Int J Mol Sci 2019; 20:4363 [View Article] [PubMed]
    [Google Scholar]
  70. Rankin DJ, Rocha EPC, Brown SP. What traits are carried on mobile genetic elements, and why?. Heredity 2011; 106:1–10 [View Article] [PubMed]
    [Google Scholar]
  71. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007; 315:1709–1712 [View Article] [PubMed]
    [Google Scholar]
  72. Bérdy J. Bioactive microbial metabolites. J Antibiot 2005; 58:1–26 [View Article] [PubMed]
    [Google Scholar]
  73. Newman DJ, Cragg GM. Natural products as sources of new drugs over the last 25 years. J Nat Prod 2007; 70:461–477 [View Article] [PubMed]
    [Google Scholar]
  74. Olano C, Méndez C, Salas JA. Antitumor compounds from marine actinomycetes. Mar Drugs 2009; 7:210–248 [View Article] [PubMed]
    [Google Scholar]
  75. Bull AT. Actinobacteria of the extremobiosphere. In Horikoshi K. eds Extremophiles Handbook Tokyo, Japan: Springer Tokyo Dordrecht Heidelberg; 2010 pp 1203–1240
    [Google Scholar]
  76. Subramani R, Sipkema D. Marine rare actinomycetes: a promising source of structurally diverse and unique novel natural products. Mar Drugs 2019; 17:E249 [View Article]
    [Google Scholar]
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