Rhodopirellula heiligendammensis sp. nov., Rhodopirellula pilleata sp. nov., and Rhodopirellula solitaria sp. nov. isolated from natural or artificial marine surfaces in Northern Germany and California, USA, and emended description of the genus Rhodopirellula

  • Nicolai Kallscheuer
  • Sandra Wiegand
  • Mareike Jogler
  • Christian Boedeker
  • Stijn H. Peeters
  • Patrick Rast
  • Anja Heuer
  • Mike S. M. Jetten
  • Manfred Rohde
  • Christian JoglerEmail author
Original Paper


Expanding the collection of Planctomycetes by characterisation of novel species is key to better understanding of their complex lifestyles, uncommon cell biology and unexplored metabolism. Here, we isolated three novel planctomycetal strains from a kelp forest on the California Coastline at Monterey Bay or from plastic surfaces submerged in the Baltic Sea and the estuary of the river Warnow in the northeast of Germany. According to our phylogenetic analysis, the isolated strains Poly21T, Pla100T and CA85T represent three novel species within the genus Rhodopirellula. All three show typical planctomycetal traits such as division by budding. All are aerobic, mesophilic chemoheterotrophs and show genomic features comparable to other described Rhodopirellula species. However, strain CA85T is exceptional as it forms cream colonies, but no aggregates, which is a notable deviation from the pink- to red-pigmented and aggregate-forming Rhodopirellula species known thus far. We propose the names Rhodopirellula heiligendammensis sp. nov., Rhodopirellula pilleata sp. nov., and Rhodopirellula solitaria sp. nov. for the novel strains Poly21T (DSM 102266T = LMG 29467T = CECT 9847T = VKM B-3435T), Pla100T (DSM 102937T = LMG 29465T) and CA85T (DSM 109595T = LMG 29699T = VKM B-3451T), respectively, which we present as the respective type strains of these novel species.


Marine bacteria Planctomycetes Rhodopirellula Baltic Sea Kelp forest Microplastic particles Monterey Bay 



Part of this research was funded by the Deutsche Forschungsgemeinschaft Grants KA 4967/1-1 and JO 893/4-1, Grant ALWOP.308 of the Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO), SIAM (Soehngen Institute for Anaerobic Microbiology) Grant No. 024002002 and the Radboud Excellence fellowship. We thank Ina Schleicher for skillful technical assistance. Brian Tindall and Regine Fähnrich from the DSMZ as well as the BCCM/LMG Bacteria collection we thank for support during strain deposition. We thank Anne-Kristin Kaster (KIT Karlsruhe, Germany) and Alfred M. Spormann (Stanford, USA) as well as the Aquarius Dive Shop Monterey and the Hopkins Marine Station for sampling support. We also thank our collaborators Sonja Oberbeckmann and Matthias Labrenz (IOW Warnemünde, Germany) for support during sampling.

Author contributions

NK wrote the manuscript and analysed the cultivation data. SW performed the genomic and phylogenetic analysis. AH, PR and MJ isolated the strains and performed the initial cultivation and strain deposition. SHP and CB performed the light microscopic analysis and prepared the LM pictures. MSMJ contributed to text preparation and revised the manuscript. MR performed the electron microscopic analysis and prepared the SEM pictures. CJ took the samples and supervised the study. All authors read and approved the final version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with animals performed by any of the authors.


  1. Acehan D, Santarella-Mellwig R, Devos DP (2013) A bacterial tubulovesicular network. J Cell Sci 127:277–280PubMedCrossRefGoogle Scholar
  2. Bengtsson MM, Øvreås L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:261PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bengtsson MM, Sjøtun K, Lanzén A, Øvreås L (2012) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6:2188–2198PubMedPubMedCentralCrossRefGoogle Scholar
  4. 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. Nucleic Acids Res 47:W81–W87PubMedPubMedCentralCrossRefGoogle Scholar
  5. Boedeker C, Schuler M, Reintjes G, Jeske O, van Teeseling MC, Jogler M, Rast P, Borchert D, Devos DP, Kucklick M, Schaffer M, Kolter R, van Niftrik L, Engelmann S, Amann R, Rohde M, Engelhardt H, Jogler C (2017) Determining the bacterial cell biology of Planctomycetes. Nat Commun 8:14853PubMedPubMedCentralCrossRefGoogle Scholar
  6. Boersma A, Kallscheuer N, Wiegand S, Rast R, Peeters S, Mesman R, Heuer A, Boedeker C, Jetten M, Rohde M, Jogler M (2019) Alienimonas californiensis gen. nov. sp. nov., a novel Planctomycete isolated from the kelp forest in Monterey Bay. Antonie van Leeuwenhoek. CrossRefGoogle Scholar
  7. Bondoso J, Harder J, Lage OM (2013) rpoB gene as a novel molecular marker to infer phylogeny in Planctomycetales. Antonie Van Leeuwenhoek 104:477–488PubMedCrossRefGoogle Scholar
  8. Bondoso J, Balague V, Gasol JM, Lage OM (2014) Community composition of the Planctomycetes associated with different macroalgae. FEMS Microbiol Ecol 88:445–456PubMedCrossRefGoogle Scholar
  9. Bondoso J, Albuquerque L, Nobre MF, Lobo-da-Cunha A, da Costa MS, Lage OM (2015) Roseimaritima ulvae gen. nov., sp. nov. and Rubripirellula obstinata gen. nov., sp. nov. two novel planctomycetes isolated from the epiphytic community of macroalgae. Syst Appl Microbiol 38:8–15PubMedCrossRefGoogle Scholar
  10. Bondoso J, Godoy-Vitorino F, Balague V, Gasol JM, Harder J, Lage OM (2017) Epiphytic Planctomycetes communities associated with three main groups of macroalgae. FEMS Microbiol Ecol 93:fiw255PubMedCentralCrossRefGoogle Scholar
  11. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedCrossRefPubMedCentralGoogle Scholar
  12. Devos DP (2014) Re-interpretation of the evidence for the PVC cell plan supports a gram-negative origin. Antonie Van Leeuwenhoek 105:271–274PubMedCrossRefPubMedCentralGoogle Scholar
  13. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedPubMedCentralCrossRefGoogle Scholar
  14. Faria M, Bordin N, Kizina J, Harder J, Devos D, Lage OM (2018) Planctomycetes attached to algal surfaces: insight into their genomes. Genomics 110:231–238PubMedCrossRefPubMedCentralGoogle Scholar
  15. Frank O, Michael V, Pauker O, Boedeker C, Jogler C, Rohde M, Petersen J (2014) Plasmid curing and the loss of grip—the 65-kb replicon of Phaeobacter inhibens DSM 17395 is required for biofilm formation, motility and the colonization of marine algae. Syst Appl Microbiol 38:120–127PubMedCrossRefPubMedCentralGoogle Scholar
  16. Fuerst JA, Webb RI (1991) Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 88:8184–8188PubMedCrossRefPubMedCentralGoogle Scholar
  17. Graca AP, Calisto R, Lage OM (2016) Planctomycetes as novel source of bioactive molecules. Front Microbiol 7:1241PubMedPubMedCentralCrossRefGoogle Scholar
  18. Ivanova AA, Naumoff DG, Miroshnikov KK, Liesack W, Dedysh SN (2017) Comparative genomics of four Isosphaeraceae planctomycetes: a common pool of plasmids and glycoside hydrolase genes shared by Paludisphaera borealis PX4T, Isosphaera pallida IS1BT, Singulisphaera acidiphila DSM 18658T, and strain SH-PL62. Front Microbiol 8:412PubMedPubMedCentralCrossRefGoogle Scholar
  19. Jeske O, Jogler M, Petersen J, Sikorski J, Jogler C (2013) From genome mining to phenotypic microarrays: Planctomycetes as source for novel bioactive molecules. Antonie Van Leeuwenhoek 104:551–567PubMedCrossRefPubMedCentralGoogle Scholar
  20. Jeske O, Schüler M, Schumann P, Schneider A, Boedeker C, Jogler M, Bollschweiler D, Rohde M, Mayer C, Engelhardt H, Spring S, Jogler C (2015) Planctomycetes do possess a peptidoglycan cell wall. Nat Commun 6:7116PubMedPubMedCentralCrossRefGoogle Scholar
  21. Jeske O, Surup F, Ketteniß M, Rast P, Förster B, Jogler M, Wink J, Jogler C (2016) Developing techniques for the utilization of Planctomycetes as producers of bioactive molecules. Front Microbiol 7:1242PubMedPubMedCentralCrossRefGoogle Scholar
  22. Jogler C (2014) The bacterial 'mitochondrium'. Mol Microbiol 94:751–755PubMedCrossRefGoogle Scholar
  23. Jogler C, Glöckner FO, Kolter R (2011) Characterization of Planctomyces limnophilus and development of genetic tools for its manipulation establish it as a model species for the phylum Planctomycetes. Appl Environ Microbiol 77:5826–5829PubMedPubMedCentralCrossRefGoogle Scholar
  24. Jogler C, Waldmann J, Huang X, Jogler M, Glöckner FO, Mascher T, Kolter R (2012) Identification of proteins likely to be involved in morphogenesis, cell division, and signal transduction in Planctomycetes by comparative genomics. J Bacteriol 194:6419–6430PubMedPubMedCentralCrossRefGoogle Scholar
  25. Kallscheuer N, Jogler M, Wiegand S, Peeters S, Heuer A, Boedeker C, Jetten M, Rohde M, Jogler C (2019a) Rubinisphaera italica sp. nov. isolated from a hydrothermal area in the Tyrrhenian Sea close to the volcanic island Panarea. Antonie van Leeuwenhoek. CrossRefPubMedGoogle Scholar
  26. Kallscheuer N, Jogler M, Wiegand S, Peeters S, Heuer A, Boedeker C, Jetten M, Rohde M, Jogler C (2019b) Three novel Rubripirellula species isolated from artificial plastic surfaces submerged in the German part of the Baltic Sea and the estuary of the river Warnow. Antonie van Leeuwenhoek. CrossRefPubMedGoogle Scholar
  27. Kallscheuer N, Moreira C, Airs R, Llewellyn CA, Wiegand S, Jogler C, Lage OM (2019c) Pink-and orange-pigmented Planctomycetes produce saproxanthin-type carotenoids including a rare C45 carotenoid. Environ Microbiol Rep 11:741–748PubMedGoogle Scholar
  28. Kallscheuer N, Wiegand S, Peeters SH, Jogler M, Boedeker C, Heuer A, Rast P, Jetten MSM, Rohde M, Jogler C (2019d) Description of three bacterial strains belonging to the new genus Novipirellula gen. nov., reclassificiation of Rhodopirellula rosea and Rhodopirellula caenicola and readjustment of the genus threshold of the phylogenetic marker rpoB for Planctomycetaceae. Antonie van Leeuwenhoek (accepted manuscript ANTO-D-19-00304)Google Scholar
  29. Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351PubMedCrossRefGoogle Scholar
  30. Kohn T, Heuer A, Jogler M, Vollmers J, Boedeker C, Bunk B, Rast P, Borchert D, Glöckner I, Freese HM, Klenk HP, Overmann J, Kaster AK, Wiegand S, Rohde M, Jogler C (2016) Fuerstia marisgermanicae gen. nov., sp. nov., an unusual member of the phylum Planctomycetes from the German Wadden Sea. Front Microbiol 7:2079PubMedPubMedCentralCrossRefGoogle Scholar
  31. Kohn T, Wiegand S, Boedeker C, Rast P, Heuer A, Jetten MSM, Schüler M, Becker S, Rohde C, Müller R-W, Brümmer F, Rohde M, Engelhardt H, Jogler M, Jogler C (2019) Planctopirus ephydatiae, a novel Planctomycete isolated from a freshwater sponge. Syst Appl Microbiol. CrossRefPubMedGoogle Scholar
  32. König E, Schlesner H, Hirsch P (1984) Cell wall studies on budding bacteria of the Planctomyces/Pasteuria group and on a Prosthecomicrobium sp. Arch Microbiol 138:200–205CrossRefGoogle Scholar
  33. Lechner M, Findeiss S, Steiner L, Marz M, Stadler PF, Prohaska SJ (2011) Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinform 12:124CrossRefGoogle Scholar
  34. Lee I, Ouk Kim Y, Park SC, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103PubMedCrossRefPubMedCentralGoogle Scholar
  35. Lindsay MR, Webb RI, Fuerst JA (1997) Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula. Microbiol UK 143:739–748CrossRefGoogle Scholar
  36. Lonhienne TG, Sagulenko E, Webb RI, Lee KC, Franke J, Devos DP, Nouwens A, Carroll BJ, Fuerst JA (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 107:12883–12888PubMedCrossRefPubMedCentralGoogle Scholar
  37. Luo C, Rodriguez RL, Konstantinidis KT (2014) MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 42:e73PubMedPubMedCentralCrossRefGoogle Scholar
  38. Neumann S, Wessels HJ, Rijpstra WI, Sinninghe Damste JS, Kartal B, Jetten MS, van Niftrik L (2014) Isolation and characterization of a prokaryotic cell organelle from the anammox bacterium Kuenenia stuttgartiensis. Mol Microbiol 94:794–802PubMedCrossRefPubMedCentralGoogle Scholar
  39. Oberbeckmann S, Kreikemeyer B, Labrenz M (2018) Environmental factors support the formation of specific bacterial assemblages on microplastics. Front Microbiol 8:2709PubMedPubMedCentralCrossRefGoogle Scholar
  40. Pilhofer M, Rappl K, Eckl C, Bauer AP, Ludwig W, Schleifer KH, Petroni G (2008) Characterization and evolution of cell division and cell wall synthesis genes in the bacterial phyla Verrucomicrobia, Lentisphaerae, Chlamydiae, and Planctomycetes and phylogenetic comparison with rRNA genes. J Bacteriol 190:3192–3202PubMedPubMedCentralCrossRefGoogle Scholar
  41. Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829PubMedPubMedCentralCrossRefGoogle Scholar
  42. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C, Zhou J, Oren A, Zhang Y-Z (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196:2210–2215PubMedPubMedCentralCrossRefGoogle Scholar
  43. Rodriguez-R LM, Konstantinidis KT (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 4:e1900v1Google Scholar
  44. Schlesner H, Rensmann C, Tindall BJ, Gade D, Rabus R, Pfeiffer S, Hirsch P (2004) Taxonomic heterogeneity within the Planctomycetales as derived by DNA–DNA hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Pirellula marina to the genus Blastopirellula gen. nov. as Blastopirellula marina comb. nov. and emended description of the genus Pirellula. Int J Syst Evol Microbiol 54:1567–1580PubMedCrossRefPubMedCentralGoogle Scholar
  45. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol Syst Biol 7:539PubMedPubMedCentralCrossRefGoogle Scholar
  46. Spring S, Bunk B, Spröer C, Schumann P, Rohde M, Tindall BJ, Klenk H-P (2016) Characterization of the first cultured representative of Verrucomicrobia subdivision 5 indicates the proposal of a novel phylum. ISME J 10:2801PubMedPubMedCentralCrossRefGoogle Scholar
  47. Stackebrandt E, Ebers J (2006) Taxonomic parameter revisited: tarnished gold standards. Microbiol Today 33:152–155Google Scholar
  48. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313PubMedPubMedCentralCrossRefGoogle Scholar
  49. van Teeseling MC, Mesman RJ, Kuru E, Espaillat A, Cava F, Brun YV, Van Nieuwenhze MS, Kartal B, van Niftrik L (2015) Anammox Planctomycetes have a peptidoglycan cell wall. Nat Commun 6:6878PubMedPubMedCentralCrossRefGoogle Scholar
  50. Vollmers J, Frentrup M, Rast P, Jogler C, Kaster AK (2017) Untangling genomes of novel planctomycetal and verrucomicrobial species from monterey bay kelp forest metagenomes by refined binning. Front Microbiol 8:472PubMedPubMedCentralCrossRefGoogle Scholar
  51. Wagner M, Horn M (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17:241–249PubMedCrossRefGoogle Scholar
  52. Wallner SR, Bauer M, Würdemann C, Wecker P, Glöckner FO, Faber K (2005) Highly enantioselective sec-alkyl sulfatase activity of the marine planctomycete Rhodopirellula baltica shows retention of configuration. Angew Chem Int Ed Engl 44:6381–6384PubMedCrossRefGoogle Scholar
  53. Wegner C-E, Richter-Heitmann T, Klindworth A, Klockow C, Richter M, Achstetter T, Glöckner FO, Harder J (2013) Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula. Mar Genomics 9:51–61PubMedCrossRefPubMedCentralGoogle Scholar
  54. Wiegand S, Jogler M, Jogler C (2018) On the maverick Planctomycetes. FEMS Microbiol Rev 42:739–760PubMedCrossRefPubMedCentralGoogle Scholar
  55. Wiegand S, Jogler M, Boedeker C, Pinto D, Vollmers J, Rivas-Marín E, Kohn T, Peeters SH, Heuer A, Rast P, Oberbeckmann S, Bunk B, Jeske O, Meyerdierks A, Storesund JE, Kallscheuer N, Lücker S, Lage OM, Pohl T, Merkel BJ, Hornburger P, Müller R-W, Brümmer F, Labrenz M, Spormann AM, Op den Camp HJM, Overmann J, Amann R, Jetten MSM, Mascher T, Medema MH, Devos DP, Kaster A-K, Øvreås L, Rohde M, Galperin MY, Jogler C (2019) Cultivation and functional characterization of 79 planctomycetes uncovers their unique biology. Nat Microbiol. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer KH, Whitman WB, Euzeby J, Amann R, Rossello-Mora R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645PubMedCrossRefPubMedCentralGoogle Scholar
  57. Žure M, Munn CB, Harder J (2015) Diversity of Rhodopirellula and related planctomycetes in a North Sea coastal sediment employing carB as molecular marker. FEMS Microbiol Lett 362:fnv127PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Nicolai Kallscheuer
    • 1
  • Sandra Wiegand
    • 1
  • Mareike Jogler
    • 1
    • 2
  • Christian Boedeker
    • 2
  • Stijn H. Peeters
    • 1
  • Patrick Rast
    • 2
  • Anja Heuer
    • 2
  • Mike S. M. Jetten
    • 1
  • Manfred Rohde
    • 3
  • Christian Jogler
    • 1
    Email author
  1. 1.Department of MicrobiologyRadboud UniversityNijmegenThe Netherlands
  2. 2.Leibniz Institute DSMZBrunswickGermany
  3. 3.Helmholtz Centre for Infection ResearchBrunswickGermany

Personalised recommendations