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Volume 72, Issue 6

sp. nov., a novel planctomycete isolated from marine sediments collected in the Portuguese north coast No Access

Abstract

The phylum is constituted by bacteria with unique features that are well adapted to a vast range of habitats. Here, we describe a novel planctomycete isolated from marine sediments collected on a beach in Matosinhos (Portugal) using an iChip-based culturing technique. Strain ICM_H10 forms beige-coloured colonies in modified M14 medium and its cells are spherical to ovoid in shape, stalked, rosette-forming and showing motility in a phase of the life cycle. Transmission electron microscopy observations showed a typical planctomycetal cell plan and cell division by budding. This strain requires salt for growth and grows in the range of 2.0–5.0 % (w/v) NaCl, from 20 to 37 °C, within a pH of 6.0–9.0 and is able to use diverse nitrogen and carbon sources. It is heterotrophic, aerobic and capable of microaerobic growth. This strain has a genome size of approximately 6.0 Mb and a G+C content of 58.1 mol%. A 16S rRNA gene-based phylogenetic analysis supports the association of strain ICM_H10 to the phylum and the family , as it shares only 96.8 and 96.4% similarity to its closest relatives Pan54 and IFAM 1448, respectively. Other phylogenetic markers also support the separation of this strain into a novel species. Morphological, physiological and genomic comparisons between strain ICM_H10 and its closest relatives strongly suggest that ICM_H10 represents a new species of the genus , for which we propose the name sp. nov., with ICM_H10 (=CECT 30326=LMG 32234) as type strain.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): beach , iChip , Matosinhos , novel taxa , Planctomycetaceae , Planctomycetota and sand
Funding
This study was supported by the:
  • Norte Portugal Regional Operational Program (NORTE 2020) (Award NORTE-01-0145-FEDER-000040)
    • Principle Award Recipient: NotApplicable
  • Fundação para a Ciência e Tecnologia (Award UIDP/04423/2020)
    • Principle Award Recipient: OlgaMaria Lage
  • Fundação para a Ciência e Tecnologia (Award UIDB/04423/2020)
    • Principle Award Recipient: OlgaMaria Lage
  • Fundação para a Ciência e Tecnologia (Award SFRH/BD/145577/2019)
    • Principle Award Recipient: InêsRosado Vitorino
© 2022 The Authors
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2022-06-10
2024-04-27
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References

  1. Oren A, Garrity GM. Valid publication of the names of forty-two phyla of prokaryotes. Int J Syst Evol Microbiol 2021; 71:10 [View Article] [PubMed]
     [Google Scholar]
  2. Lage OM, van Niftrik L, Jogler C, Devos DP. Planctomycetes. In Schmidt TM. eds Encyclopedia of Microbiology, 4th edn. Oxford: Academic Press; 2019 pp 614–626
     [Google Scholar]
  3. Slobodkina GB, Kovaleva OL, Miroshnichenko ML, Slobodkin AI, Kolganova TV et al. Thermogutta terrifontis gen. nov., sp. nov. and Thermogutta hypogea sp. nov., thermophilic anaerobic representatives of the phylum Planctomycetes. Int J Syst Evol Microbiol 2015; 65:760–765 [View Article]
     [Google Scholar]
  4. Wiegand S, Jogler M, Boedeker C, Pinto D, Vollmers J et al. Cultivation and functional characterization of 79 planctomycetes uncovers their unique biology. Nat Microbiol 2020; 5:126–140 [View Article] [PubMed]
     [Google Scholar]
  5. Dedysh SN, Ivanova AA. Planctomycetes in boreal and subarctic wetlands: diversity patterns and potential ecological functions. FEMS Microbiol Ecol 2019; 95: [View Article] [PubMed]
     [Google Scholar]
  6. Bondoso J, Balagué V, Gasol JM, Lage OM. Community composition of the planctomycetes associated with different macroalgae. FEMS Microbiol Ecol 2014; 88:445–456 [View Article] [PubMed]
     [Google Scholar]
  7. Lage OM, Bondoso J. Planctomycetes and macroalgae, a striking association. Front Microbiol 2014; 5:267 [View Article] [PubMed]
     [Google Scholar]
  8. Lage OM, Bondoso J. Planctomycetes diversity associated with macroalgae. FEMS Microbiol Ecol 2011; 78:366–375 [View Article] [PubMed]
     [Google Scholar]
  9. Wiegand S, Rast P, Kallscheuer N, Jogler M, Heuer A et al. Analysis of bacterial communities on north sea macroalgae and characterization of the isolated planctomycetes Adhaeretor mobilis gen. nov., sp. nov., Roseimaritima multifibrata sp. nov., Rosistilla ulvae sp. nov. and Rubripirellula lacrimiformis sp. nov. Microorganisms 2021; 9:1494 [View Article]
     [Google Scholar]
  10. Bengtsson MM, Øvreås L. Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 2010; 10:261 [View Article] [PubMed]
     [Google Scholar]
  11. Izumi H, Sagulenko E, Webb RI, Fuerst JA. Isolation and diversity of planctomycetes from the sponge Niphates sp., seawater, and sediment of Moreton Bay, Australia. Antonie van Leeuwenhoek 2013; 104:533–546 [View Article] [PubMed]
     [Google Scholar]
  12. Kallscheuer N, Wiegand S, Kohn T, Boedeker C, Jeske O et al. Cultivation-independent analysis of the bacterial community associated with the calcareous sponge Clathrina clathrus and isolation of Poriferisphaera corsica gen. nov., sp. nov., belonging to the barely studied class Phycisphaerae in the phylum Planctomycetes. Front Microbiol 2020; 11:602250 [View Article]
     [Google Scholar]
  13. Kohn T, Wiegand S, Boedeker C, Rast P, Heuer A et al. Planctopirus ephydatiae, a novel planctomycete isolated from a freshwater sponge. Syst Appl Microbiol 2020; 43:126022 [View Article] [PubMed]
     [Google Scholar]
  14. Kumar G, Kumar D, Jagadeeshwari U, Sreya PK, Shabbir A et al. Crateriforma spongiae sp. nov., isolated from a marine sponge and emended description of the genus “Crateriforma”. Antonie van Leeuwenhoek 2021; 114:341–353 [View Article] [PubMed]
     [Google Scholar]
  15. Kohn T, Heuer A, Jogler M, Vollmers J, Boedeker C et al. Corrigendum: Fuerstia marisgermanicae gen. nov., sp. nov., an unusual member of the phylum Planctomycetes from the German Wadden Sea. Front Microbiol 2019; 10:1029 [View Article]
     [Google Scholar]
  16. Kohn T, Heuer A, Jogler M, Vollmers J, Boedeker C et al. Fuerstia marisgermanicae gen. nov., sp. nov., an unusual member of the phylum Planctomycetes from the German Wadden Sea. Front Microbiol 2016; 7:2079 [View Article]
     [Google Scholar]
  17. Boedeker C, Schüler M, Reintjes G, Jeske O, van Teeseling MCF et al. Determining the bacterial cell biology of Planctomycetes. Nat Commun 2017; 8:14853 [View Article] [PubMed]
     [Google Scholar]
  18. Jeske O, Schüler M, Schumann P, Schneider A, Boedeker C et al. Planctomycetes do possess a peptidoglycan cell wall. Nat Commun 2015; 6:7116 [View Article] [PubMed]
     [Google Scholar]
  19. Rivas-Marín E, Devos DP. The paradigms they are a-changin’: past, present and future of PVC bacteria research. Antonie van Leeuwenhoek 2018; 111:785–799 [View Article] [PubMed]
     [Google Scholar]
  20. Wiegand S, Jogler M, Jogler C. On the maverick Planctomycetes. FEMS Microbiol Rev 2018; 42:739–760 [View Article] [PubMed]
     [Google Scholar]
  21. 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]
  22. Graça AP, Calisto R, Lage OM. Planctomycetes as novel source of bioactive molecules. Front Microbiol 2016; 7:1241 [View Article] [PubMed]
     [Google Scholar]
  23. Jeske O, Jogler M, Petersen J, Sikorski J, Jogler C. From genome mining to phenotypic microarrays: planctomycetes as source for novel bioactive molecules. Antonie van Leeuwenhoek 2013; 104:551–567 [View Article] [PubMed]
     [Google Scholar]
  24. Jeske O, Surup F, Ketteniß M, Rast P, Förster B et al. Developing techniques for the utilization of planctomycetes as producers of bioactive molecules. Front Microbiol 2016; 7:1242 [View Article] [PubMed]
     [Google Scholar]
  25. Belova SE, Saltykova VA, Dedysh SN. Antimicrobial activity of a novel freshwater planctomycete Lacipirellula parvula PX69T. Microbiology 2020; 89:503–509 [View Article]
     [Google Scholar]
  26. Sandargo B, Jeske O, Boedeker C, Wiegand S, Wennrich J-P et al. Stieleriacines, N-Acyl dehydrotyrosines from the marine planctomycete Stieleria neptunia sp. nov. Front Microbiol 2020; 11:1408 [View Article]
     [Google Scholar]
  27. Kallscheuer N, Jeske O, Sandargo B, Boedeker C, Wiegand S et al. The planctomycete Stieleria maiorica Mal15T employs stieleriacines to alter the species composition in marine biofilms. Commun Biol 2020; 3:303 [View Article] [PubMed]
     [Google Scholar]
  28. Calisto R, Sæbø EF, Storesund JE, Øvreås L, Herfindal L et al. Anticancer activity in planctomycetes. Front Mar Sci 2019; 5:499 [View Article]
     [Google Scholar]
  29. Gimranov E, Santos JDN, Vitorino I, Martín J, Reyes F et al. Marine bacterial activity against phytopathogenic Pseudomonas show high efficiency of Planctomycetes extracts. Eur J Plant Pathol 2022; 162:843–854 [View Article]
     [Google Scholar]
  30. Vitorino IR, Lage OM. The Planctomycetia: an overview of the currently largest class within the phylum Planctomycetes. Antonie van Leeuwenhoek 2022; 115:169–201 [View Article] [PubMed]
     [Google Scholar]
  31. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41:D590–6 [View Article] [PubMed]
     [Google Scholar]
  32. 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]
  33. Dedysh SN, Henke P, Ivanova AA, Kulichevskaya IS, Philippov DA et al. 100-year-old enigma solved: identification, genomic characterization and biogeography of the yet uncultured Planctomyces bekefii. Environ Microbiol 2020; 22:198–211 [View Article] [PubMed]
     [Google Scholar]
  34. Kovaleva OL, Elcheninov AG, Toshchakov SV, Novikov AA, Bonch-Osmolovskaya EA et al. Tautonia sociabilis gen. nov., sp. nov., a novel thermotolerant planctomycete, isolated from a 4000 m deep subterranean habitat. Int J Syst Evol Microbiol 2019; 69:2299–2304 [View Article]
     [Google Scholar]
  35. Kulichevskaya IS, Naumoff DG, Miroshnikov KK, Ivanova AA, Philippov DA et al. Limnoglobus roseus gen. nov., sp. nov., a novel freshwater planctomycete with a giant genome from the family Gemmataceae. Int J Syst Evol Microbiol 2020; 70:1240–1249 [View Article]
     [Google Scholar]
  36. Pradel N, Fardeau ML, Tindall BJ, Spring S. Anaerohalosphaera lusitana gen. nov., sp. nov., and Limihaloglobus sulfuriphilus gen. nov., sp. nov., isolated from solar saltern sediments, and proposal of Anaerohalosphaeraceae fam. nov. within the order Sedimentisphaerales. Int J Syst Evol Microbiol 2020; 70:1321–1330 [View Article]
     [Google Scholar]
  37. Dedysh SN, Beletsky AV, Ivanova AA, Kulichevskaya IS, Suzina NE et al. Wide distribution of Phycisphaera-like planctomycetes from WD2101 soil group in peatlands and genome analysis of the first cultivated representative. Environ Microbiol 2021; 23:1510–1526 [View Article] [PubMed]
     [Google Scholar]
  38. Gaurav K, Kumar D, Jagadeeshwari U, Shabbir A, Sasikala C et al. Phylo-taxogenomics of the genus Tautonia with descriptions of Tautonia marina sp. nov., Tautonia rosea sp. nov., and emended description of the genus. Syst Appl Microbiol 2021; 44:126229 [View Article]
     [Google Scholar]
  39. Godinho O, Botelho R, Albuquerque L, Wiegand S, Kallscheuer N et al. Bremerella alba sp. nov., a novel planctomycete isolated from the surface of the macroalga Fucus spiralis. Syst Appl Microbiol 2021; 44:126189 [View Article] [PubMed]
     [Google Scholar]
  40. Kulichevskaya IS, Ivanova AA, Naumoff DG, Beletsky AV, Rijpstra WIC et al. Frigoriglobus tundricola gen. nov., sp. nov., a psychrotolerant cellulolytic planctomycete of the family Gemmataceae from a littoral tundra wetland. Syst Appl Microbiol 2020; 43:126129 [View Article]
     [Google Scholar]
  41. Kumar D, Gaurav K, Pk S, A S, Uppada J et al. Gimesia chilikensis sp. nov., a haloalkali-tolerant planctomycete isolated from Chilika lagoon and emended description of the genus Gimesia. Int J Syst Evol Microbiol 2020; 70:3647–3655 [View Article] [PubMed]
     [Google Scholar]
  42. Kumar D, Gaurav K, U J, G D, Ch. S et al. Roseimaritima sediminicola sp. nov., a new member of Planctomycetaceae isolated from Chilika lagoon. Int J Syst Evol Microbiol 2020; 70:2616–2623 [View Article] [PubMed]
     [Google Scholar]
  43. Vitorino I, Albuquerque L, Wiegand S, Kallscheuer N, da Costa MS et al. Alienimonas chondri sp. nov., a novel planctomycete isolated from the biofilm of the red alga Chondrus crispus. Syst Appl Microbiol 2020; 43:126083 [View Article] [PubMed]
     [Google Scholar]
  44. Vitorino I, Albuquerque L, Wiegand S, Kallscheuer N, da Costa MS et al. Corrigendum to “Alienimonas chondri sp. nov., a novel planctomycete isolated from the biofilm of the red alga Chondrus crispus” [Syst. Appl. Microbiol. 43 (2020) 126083]. Syst Appl Microbiol 2021; 44:126219 [View Article] [PubMed]
     [Google Scholar]
  45. Kumar G, Lhingjakim KL, Uppada J, Ahamad S, Kumar D et al. Aquisphaera insulae sp. nov., a new member in the family Isosphaeraceae, isolated from the floating island of Loktak lake and emended description of the genus Aquisphaera. Antonie van Leeuwenhoek 2021; 114:1465–1477 [View Article] [PubMed]
     [Google Scholar]
  46. Vitorino I, Santos JDN, Godinho O, Vicente F, Vasconcelos V et al. Novel and conventional isolation techniques to obtain planctomycetes from marine environments. Microorganisms 2021; 9:2078 [View Article]
     [Google Scholar]
  47. Dedysh SN, Kulichevskaya IS, Beletsky AV, Ivanova AA, Rijpstra WIC et al. Lacipirellula parvula gen. nov., sp. nov., representing a lineage of planctomycetes widespread in low-oxygen habitats, description of the family Lacipirellulaceae fam. nov. and proposal of the orders Pirellulales ord. nov., Gemmatales ord. nov. and Isosphaerales ord. nov. Syst Appl Microbiol 2020; 43:126050 [View Article]
     [Google Scholar]
  48. Nichols D, Cahoon N, Trakhtenberg EM, Pham L, Mehta A et al. Use of ichip for high-throughput in situ cultivation of “uncultivable” microbial species. Appl Environ Microbiol 2010; 76:2445–2450 [View Article] [PubMed]
     [Google Scholar]
  49. 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]
  50. 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]
  51. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article]
     [Google Scholar]
  52. Kumar S, Stecher G, Li M, Knyaz C, Tamura K et al. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
     [Google Scholar]
  53. Scheuner C, Tindall BJ, Lu M, Nolan M, Lapidus A et al. Complete genome sequence of Planctomyces brasiliensis type strain (DSM 5305(T)), phylogenomic analysis and reclassification of Planctomycetes including the descriptions of Gimesia gen. nov., Planctopirus gen. nov. and Rubinisphaera gen. nov. and emended descriptions of the order Planctomycetales and the family Planctomycetaceae. Stand Genomic Sci 2014; 9:10 [View Article]
     [Google Scholar]
  54. Schlesner H. Planctomyces brasiliensis sp. nov., a halotolerant bacterium from a salt pit. Syst Appl Microbiol 1989; 12:159–161 [View Article]
     [Google Scholar]
  55. Kallscheuer N, Jogler M, Wiegand S, Peeters SH, Heuer A et al. Rubinisphaera italica sp. nov. isolated from a hydrothermal area in the Tyrrhenian Sea close to the volcanic island Panarea. Antonie van Leeuwenhoek 2019; 113:1727–1736 [View Article] [PubMed]
     [Google Scholar]
  56. 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]
  57. Li W, O’Neill KR, Haft DH, DiCuccio M, Chetvernin V et al. RefSeq: expanding the Prokaryotic Genome Annotation Pipeline reach with protein family model curation. Nucleic Acids Res 2021; 49:D1020–D1028 [View Article] [PubMed]
     [Google Scholar]
  58. Haft DH, DiCuccio M, Badretdin A, Brover V, Chetvernin V et al. RefSeq: an update on prokaryotic genome annotation and curation. Nucleic Acids Res 2018; 46:D851–D860 [View Article] [PubMed]
     [Google Scholar]
  59. Souvorov A, Agarwala R, Lipman DJ. SKESA: strategic k-mer extension for scrupulous assemblies. Genome Biol 2018; 19:153 [View Article] [PubMed]
     [Google Scholar]
  60. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
     [Google Scholar]
  61. Lee I, Chalita M, Ha S-M, Na S-I, Yoon S-H et al. ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int J Syst Evol Microbiol 2017; 67:2053–2057 [View Article] [PubMed]
     [Google Scholar]
  62. 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] [PubMed]
     [Google Scholar]
  63. Yoon SH, Ha SM, 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]
  64. 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]
  65. Medlar AJ, Törönen P, Holm L. AAI-profiler: fast proteome-wide exploratory analysis reveals taxonomic identity, misclassification and contamination. Nucleic Acids Res 2018; 46:W479–W485 [View Article] [PubMed]
     [Google Scholar]
  66. 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]
  67. Kallscheuer N, Jogler C. The bacterial phylum Planctomycetes as novel source for bioactive small molecules. Biotechnol Adv 2021; 53:107818 [View Article] [PubMed]
     [Google Scholar]
  68. 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]
  69. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article] [PubMed]
     [Google Scholar]
  70. 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]
  71. 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]
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Rubinisphaera margarita sp. nov., a novel planctomycete isolated from marine sediments collected in the Portuguese north coast
Int J Syst Evol Microbiol 72, 005425 (2022); https://doi.org/10.1099/ijsem.0.005425
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