Advertisement

Antonie van Leeuwenhoek

, Volume 111, Issue 11, pp 2095–2105 | Cite as

Assembly of a complete genome sequence for Gemmata obscuriglobus reveals a novel prokaryotic rRNA operon gene architecture

  • Josef D. Franke
  • Wilson R. Blomberg
  • Robert T. Todd
  • Robert W. Thomas
  • Anna M. Selmecki
Original Paper

Abstract

Gemmata obscuriglobus is a Gram-negative bacterium with several intriguing biological features. Here, we present a complete, de novo whole genome assembly for G. obscuriglobus which consists of a single, circular 9 Mb chromosome, with no plasmids detected. The genome was annotated using the NCBI Prokaryotic Genome Annotation pipeline to generate common gene annotations. Analysis of the rRNA genes revealed three interesting features for a bacterium. First, linked G. obscuriglobus rrn operons have a unique gene order, 23S–5S–16S, compared to typical prokaryotic rrn operons (16S–23S–5S). Second, G. obscuriglobus rrn operons can either be linked or unlinked (a 16S gene is in a separate genomic location from a 23S and 5S gene pair). Third, all of the 23S genes (5 in total) have unique polymorphisms. Genome analysis of a different Gemmata species (SH-PL17), revealed a similar 23S–5S–16S gene order in all of its linked rrn operons and the presence of an unlinked operon. Together, our findings show that unique and rare features in Gemmata rrn operons among prokaryotes provide a means to better define the evolutionary relatedness of Gemmata species and the divergence time for different Gemmata species. Additionally, these rrn operon differences provide important insights into the rrn operon architecture of common ancestors of the planctomycetes.

Keywords

PVC superphylum Planctomycete De novo genome assembly rrn operon Phylogenetics 

Notes

Acknowledgements

We would like to thank Drs. Jill Blankenship and Chuck Deutch for comments on the manuscript and Curtis Focht for assistance with bioinformatic programming.

Funding

This work is supported by a Nebraska LB692 Tobacco Settlement Biomedical Research Development Award and a Nebraska Established Program to Stimulate Competitive Research (EPSCoR) First Award to A.M.S., a Creighton University Ferlic Summer Undergraduate Research Fellowship to W.R.B., and a Creighton University CURAS Faculty Research Fund Award to J.D.F.

Compliance with ethical standards

Conflict of interest

None of the authors have any competing financial conflicts of interests.

References

  1. Aghnatios R, Cayrou C, Garibal M, Robert C, Azza S, Raoult D, Drancourt M (2015) Draft genome of Gemmata massiliana sp. nov, a water-borne Planctomycetes species exhibiting two variants. Stand Genomic Sci 10:120.  https://doi.org/10.1186/s40793-015-0103-0 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Andersson SG, Stothard DR, Fuerst P, Kurland CG (1999) Molecular phylogeny and rearrangement of rRNA genes in Rickettsia species. Mol Biol Evol 16:987–995.  https://doi.org/10.1093/oxfordjournals.molbev.a026188 CrossRefPubMedGoogle Scholar
  3. Boedeker C et al (2017) Determining the bacterial cell biology of Planctomycetes. Nat Commun 8:14853.  https://doi.org/10.1038/ncomms14853 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120.  https://doi.org/10.1093/bioinformatics/btu170 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cejkova D, Zobanikova M, Pospisilova P, Strouhal M, Mikalova L, Weinstock GM, Smajs D (2013) Structure of rrn operons in pathogenic non-cultivable treponemes: sequence but not genomic position of intergenic spacers correlates with classification of Treponema pallidum and Treponema paraluiscuniculi strains. J Med Microbiol 62:196–207.  https://doi.org/10.1099/jmm.0.050658-0 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797.  https://doi.org/10.1093/nar/gkh340 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Glockner FO et al (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100:8298–8303.  https://doi.org/10.1073/pnas.1431443100 CrossRefPubMedGoogle Scholar
  8. Goker M et al (2011) Complete genome sequence of Isosphaera pallida type strain (IS1B). Stand Genomic Sci 4:63–71.  https://doi.org/10.4056/sigs.1533840 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Gottshall EY, Seebart C, Gatlin JC, Ward NL (2014) Spatially segregated transcription and translation in cells of the endomembrane-containing bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 111:11067–11072.  https://doi.org/10.1073/pnas.1409187111 CrossRefPubMedGoogle Scholar
  10. Green JL, Bohannan BJ, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:1039–1043.  https://doi.org/10.1126/science.1153475 CrossRefPubMedGoogle Scholar
  11. Guo M et al (2012) Genome sequences of three species in the family Planctomycetaceae. J Bacteriol 194:3740–3741.  https://doi.org/10.1128/JB.00639-12 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Hartmann RK, Erdmann VA (1989) Thermus thermophilus 16S rRNA is transcribed from an isolated transcription unit. J Bacteriol 171:2933–2941CrossRefGoogle Scholar
  13. 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 PX4(T), Isosphaera pallida IS1B(T), Singulisphaera acidiphila DSM 18658(T), and strain SH-PL62. Front Microbiol 8:412.  https://doi.org/10.3389/fmicb.2017.00412 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Klappenbach JA, Dunbar JM, Schmidt TM (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66:1328–1333CrossRefGoogle Scholar
  15. Kulichevskaya IS, Ivanova AA, Suzina NE, Rijpstra WIC, Sinninghe Damste JS, Dedysh SN (2016) Paludisphaera borealis gen. nov., sp. nov., a hydrolytic planctomycete from northern wetlands, and proposal of Isosphaeraceae fam. nov. Int J Syst Evol Microbiol 66:837–844.  https://doi.org/10.1099/ijsem.0.000799 CrossRefPubMedGoogle Scholar
  16. Lee KC, Webb RI, Fuerst JA (2009) The cell cycle of the planctomycete Gemmata obscuriglobus with respect to cell compartmentalization. BMC Cell Biol 10:4.  https://doi.org/10.1186/1471-2121-10-4 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26:589–595.  https://doi.org/10.1093/bioinformatics/btp698 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Li D, Leahy S, Henderson G, Kelly W, Cookson A, Attwood G, Moon C (2014) Atypical bacterial rRNA operon structure is prevalent within the Lachnospiraceae, and use of the 16S–23S rRNA internal transcribed spacer region for the rapid identification of ruminal Butyrivibrio and Pseudobutyrivibrio strains. Ann Microbiol 64:1623–1631.  https://doi.org/10.1007/s13213-014-0806-2 CrossRefGoogle Scholar
  19. Lieber A, Leis A, Kushmaro A, Minsky A, Medalia O (2009) Chromatin organization and radio resistance in the bacterium Gemmata obscuriglobus. J Bacteriol 191:1439–1445.  https://doi.org/10.1128/JB.01513-08 CrossRefPubMedGoogle Scholar
  20. Liesack W, Stackebrandt E (1989) Evidence for unlinked rrn operons in the Planctomycete Pirellula marina. J Bacteriol 171:5025–5030CrossRefGoogle Scholar
  21. Lonhienne TG et al (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 107:12883–12888.  https://doi.org/10.1073/pnas.1001085107 CrossRefPubMedGoogle Scholar
  22. Menke MAOH, Liesack W, Stackebrandt E (1991) Ribotyping of 16S and 23S rRNA genes and organization of rrn operons in members of the bacterial genera Gemmata, Planctomyces, Thermotoga, Thermus, and Verrucomicrobium. Arch Microbiol 155:263–271.  https://doi.org/10.1007/BF00252210 CrossRefGoogle Scholar
  23. Mishek HP, Stock SA, Florick JDE, Blomberg WR, Franke JD (2018) Development of a chemically-defined minimal medium for studies on growth and protein uptake of Gemmata obscuriglobus. J Microbiol Methods 145:40–46.  https://doi.org/10.1016/j.mimet.2017.12.010 CrossRefPubMedGoogle Scholar
  24. Pearson A, Budin M, Brocks JJ (2003) Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 100:15352–15357.  https://doi.org/10.1073/pnas.2536559100 CrossRefPubMedGoogle Scholar
  25. Pei A, Nossa CW, Chokshi P, Blaser MJ, Yang L, Rosmarin DM, Pei Z (2009) Diversity of 23S rRNA genes within individual prokaryotic genomes. PLoS ONE 4:e5437.  https://doi.org/10.1371/journal.pone.0005437 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Rivas-Marin E, Canosa I, Devos DP (2016) Evolutionary cell biology of division mode in the bacterial Planctomycetes–Verrucomicrobia–Chlamydiae superphylum. Front Microbiol 7:1964.  https://doi.org/10.3389/fmicb.2016.01964 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26.  https://doi.org/10.1038/nbt.1754 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Sagulenko E, Morgan GP, Webb RI, Yee B, Lee KC, Fuerst JA (2014) Structural studies of planctomycete Gemmata obscuriglobus support cell compartmentalisation in a bacterium. PLoS ONE 9:e91344.  https://doi.org/10.1371/journal.pone.0091344 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Santarella-Mellwig R, Pruggnaller S, Roos N, Mattaj IW, Devos DP (2013) Three-dimensional reconstruction of bacteria with a complex endomembrane system. PLoS Biol 11:e1001565.  https://doi.org/10.1371/journal.pbio.1001565 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Scheuner C et al (2014) 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 9:10.  https://doi.org/10.1186/1944-3277-9-10 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Shrestha PM, Noll M, Liesack W (2007) Phylogenetic identity, growth-response time and rRNA operon copy number of soil bacteria indicate different stages of community succession. Environ Microbiol 9:2464–2474.  https://doi.org/10.1111/j.1462-2920.2007.01364.x CrossRefPubMedGoogle Scholar
  32. Staley JT, Fuerst JA, Giovannoni S, Schlesner H (1992) The order Planctomycetales and the genera Planctomyces, Pirellula, Gemmata and Isosphaera. In: Ballows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, New YorkGoogle Scholar
  33. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Thorvaldsdottir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192.  https://doi.org/10.1093/bib/bbs017 CrossRefGoogle Scholar
  35. van Niftrik L, Devos DP (2017) Editorial: Planctomycetes–Verrucomicrobia–Chlamydiae bacterial superphylum: new model organisms for evolutionary cell biology. Front Microbiol 8:1458.  https://doi.org/10.3389/fmicb.2017.01458 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Walker BJ et al (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9:e112963.  https://doi.org/10.1371/journal.pone.0112963 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ward NL, Rainey FA, Hedlund BP, Staley JT, Ludwig W, Stackebrandt E (2000) Comparative phylogenetic analyses of members of the order Planctomycetales and the division Verrucomicrobia: 23S rRNA gene sequence analysis supports the 16S rRNA gene sequence-derived phylogeny. Int J Syst Evol Microbiol 50(Pt 6):1965–1972.  https://doi.org/10.1099/00207713-50-6-1965 CrossRefPubMedGoogle Scholar
  38. Yap WH, Zhang Z, Wang Y (1999) Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J Bacteriol 181:5201–5209PubMedPubMedCentralGoogle Scholar
  39. Yee B, Sagulenko E, Morgan GP, Webb RI, Fuerst JA (2012) Electron tomography of the nucleoid of Gemmata obscuriglobus reveals complex liquid crystalline cholesteric structure. Front Microbiol 3:326.  https://doi.org/10.3389/fmicb.2012.00326 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyCreighton UniversityOmahaUSA
  2. 2.Department of Medical Microbiology and ImmunologyCreighton University Medical SchoolOmahaUSA

Personalised recommendations