Skip to main content
SpringerLink
Log in

New insights into the metabolic potential of the phototrophic purple bacterium Rhodopila globiformis DSM 161T from its draft genome sequence and evidence for a vanadium-dependent nitrogenase

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Rhodopila globiformis: is the most acidophilic anaerobic anoxygenic phototrophic purple bacterium and was isolated from a warm acidic sulfur spring in Yellowstone Park. Its genome is larger than genomes of other phototrophic purple bacteria, containing 7248 Mb with a G + C content of 67.1% and 6749 protein coding and 53 RNA genes. The genome revealed some previously unknown properties such as the presence of two sets of structural genes pufLMC for the photosynthetic reaction center genes and two types of nitrogenases (Mo-Fe and V-Fe nitrogenase), capabilities of autotrophic carbon dioxide fixation and denitrification using nitrite. Rhodopila globiformis assimilates sulfate and utilizes the C1 carbon substrates CO and methanol and a number of organic compounds, in particular, sugars and aromatic compounds. It is among the few purple bacteria containing a large number of pyrroloquinoline quinone-dependent dehydrogenases. It has extended capacities to resist stress by heavy metals, demonstrates different resistance mechanisms to antibiotics, and employs several toxin/antitoxin systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alberti M, Burke DH, Hearst JE (1995) Structure and sequence of the photosynthesis gene cluster. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publications, Dordrecht, pp 1083–1106

    Google Scholar 

  • Ambler RP, Meyer TE, Cusanovich MA, Kamen MD (1987) The amino acid sequence of the cytochrome c2 from the phototrophic bacterium Rhodopseudomonas globiformis. Biochemical J 246:115–120

    Article  CAS  Google Scholar 

  • Ambler RP, Meyer TE, Kamen MD (1993) Amino acid sequence of a high redox potential ferredoxin (HiPIP) from the purple phototrophic bacterium, Rhodopila globiformis, which has the highest known redox potential of its class. Arch Biochem Biophys 306:215–222

    Article  PubMed  CAS  Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA et al (2008) The RAST Server: Rapid Annotations using Subsystems Technology. BMC Genom 9:75

    Article  CAS  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Benning MM, Meyer TE, Holden HM (1996) Molecular structure of a high-potential cytochrome c2 isolated from Rhodopila globiformis. Arch Biochem Biophys 333:338–348

    Article  PubMed  CAS  Google Scholar 

  • Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27:578–579

    Article  PubMed  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bradnam KR, Fass JN, Alexandrov A, Baranay P, Bechner M, Birol I et al (2013) Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species. GigaScience 2:1. https://doi.org/10.1186/2047-217X-2-10

    Article  CAS  Google Scholar 

  • Bushnell B (2016) BBMap short read aligner for DNA/RNAseq. Walnut Creek, CA. https://sourceforge.net/projects/bbmap

  • Fisher K, Diworth MJ, Newton WE (2006) Azotobacter vinelandii vanadium nitrogenase: formaldehyde is a product of catalyzed HCN reduction and excess ammonia arises directly from catalyzed azide reduction. Biochem 45:4190–4198

    Article  CAS  Google Scholar 

  • Hensel G, Trüper HG (1976) Cysteine and S-sulfocysteine biosynthesis in phototrophic bacteria. Arch Microbiol 109:101–103

    Article  PubMed  CAS  Google Scholar 

  • Hiraishi A, Imhoff JF (2005) Acidiphilium. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology. Volume 2: The Proteobacteria. Part C: The alpha-, beta-, delta-, and epsilonproteobacteria, vol 2, 2nd edn. Springer, New York, pp 54–62

    Chapter  Google Scholar 

  • Hiraishi A, Shimada K (2001) Aerobic anoxygenic photosynthetic bacteria with zinc-bacteriochlorophyll. J Gen Appl Microbiol 47:161–180

    Article  PubMed  CAS  Google Scholar 

  • Hiraishi A, Matsuzawa Y, Kanbe T et al (2000) Acidisphaera rubrifaciens, gen. nov., sp. nov., an aerobic bacteriochlorophyll-containing bacterium isolated from acidic environments. Int J Syst Evol Microbiol 50:1539–1546

    Article  PubMed  CAS  Google Scholar 

  • Imhoff JF (2005) Rhodoblastus. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology. Volume 2: The proteobacteria. Part C: The alpha-, beta-, delta-, and epsilonproteobacteria, vol 2, 2nd edn. Springer, New York, pp 471–473  

    Chapter  Google Scholar 

  • Imhoff JF (2017) Diversity of anaerobic anoxygenic phototrophic purple bacteria. In: Hallenbeck P (ed) Modern topics in the phototrophic prokaryotes: environmental and applied aspects, chap 2. Springer, Cham, pp 47–85

    Chapter  Google Scholar 

  • Imhoff JF, Then J, Hashwa F et al (1981) Sulfate assimilation in Rhodopseudomonas globiformis. Arch Microbiol 130:234–237

    Article  CAS  Google Scholar 

  • Imhoff JF, Trüper HG, Pfennig N (1984) Rearrangement of the species and genera of the phototrophic purple nonsulfur bacteria. Int J Syst Bacteriol 34:340–343

    Article  Google Scholar 

  • Jacobson MR, Premnakumar R, Bishop PE (1986) Transcriptional regulation of nitrogen fixation by molybdenum in Azotobacter vinelandii. J Bacteriol 167:480–486

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jiao N, Zhang R, Zheng Q (2010) Coexistence oft wo different photosynthetic operons in Citromicrobium bathyomarinum JL354 as revealed by whole-genome sequencing. J Bacteriol 192:1169–1170

    Article  PubMed  CAS  Google Scholar 

  • Kang DD, Froula J, Egan R, Wang Z (2014) A robust statistical framework for reconstructing genomes from metagenomic data. bioRxiv. https://doi.org/10.1101/011460

    Article  Google Scholar 

  • Kobayashi M, Yamamura M, Akiyama M, Kise H, Inoue K, Hara M, Wakao N, Yahara K, Watanabe T (1998) Acid resistance of Zn-bacteriochlorophyll a from an acidophilic bacterium Acidiphilium rubrum. Anal Sci 14:1149–1152

    Article  CAS  Google Scholar 

  • Kulichevskaya IS, Guzev VS, Gorlenko VM, Liesack W, Svetlana N, Dedysh SN (2006) Rhodoblastus sphagnicola sp. nov., a novel acidophilic purple non-sulfur bacterium from Sphagnum peat bog. Intern J Syst Evol Microbiol 56:1397–1402. https://doi.org/10.1099/ijs.0.63962-0

    Article  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Madigan M, Cox SS (1982) Nitrogen metabolism in Rhodopseudomonas globiformis. Arch Microbiol 133:6–10

    Article  CAS  Google Scholar 

  • Masuda T, Inoue K, Masuda M, Nagayama M, Tamaki A, Ohta H, Shimada H, Takamiya K (1999) Magnesium insertion by magnesium chelatase in the biosynthesis of zinc bacteriochlorophyll a in an aerobic acidophilic bacterium Acidiphilium rubrum. J Biol Chem 274:33594–33600

    Article  PubMed  CAS  Google Scholar 

  • Morgulis A, Gertz EM, Schäffer AA, Agarwala R (2006) A fast and symmetric DUST implementation to mask low-complexity DNA sequences. J Comput Biol 13:1028–1040

    Article  PubMed  CAS  Google Scholar 

  • Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A, Lapidus A et al (2013) Assembling genomes and mini-metagenomes from highly chimeric reads. In: Deng M, Jiang R, Sun F, Zhang X (eds) Research in computational molecular biology. Springer, Heidelberg, pp 158–170

    Chapter  Google Scholar 

  • Oda Y, Samanta SK, Rey FE, Wu L, Liu X, Yan T, Zhou J, Harwood CS (2005) Functional genomic analysis of three nitrogenase isoenzymes in the photosynthetic bacterium Rhodopseudomonas palustris. J Bacteriol 187:7784–7794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Okamura K, Hisada T, Kanbe T, Hiraishi A (2009) Rhodovastum atsumiense gen. nov., sp. nov., a phototrophic alphaproteobacterium isolated from paddy soil. J Gen Appl Microbiol 55:43–50

    Article  PubMed  CAS  Google Scholar 

  • Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T et al (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42:D206–D214. https://doi.org/10.1093/nar/gkt1226

    Article  PubMed  CAS  Google Scholar 

  • Perrière G, Gouy M (1996) WWW-Query: An on-line retrieval system for biological sequence banks. Biochimie 78:364–369

    Article  PubMed  Google Scholar 

  • Pfennig N (1974) Rhodopseudomonas globiformis, sp. n., a new species of the Rhodospirillaceae. Arch Microbiol 100:197–206

    Article  CAS  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Shaik S, Kumar N, Lankapalli AK, Tiwari SK, Baddam R, Ahmed N (2016) Contig-Layout-Authenticator (CLA): A combinatorial approach to ordering and scaffolding of bacterial contigs for comparative genomics and molecular epidemiology. PLoS One 11:e0155459. https://doi.org/10.1371/journal.pone.0155459

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Then J, Trüper HG (1981) The role of thiosulfate in sulfur metabolism of Rhodopseudomonas globiformis. Arch Microbiol 130:143–146

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. GEOMAR Helmholtz Center for Ocean Research Kiel, Düsternbrooker Weg 20, 24105, Kiel, Germany

    Johannes F. Imhoff & Tanja Rahn

  2. Max Planck Institut für Evolutionsbiologie, 24306, Plön, Germany

    Sven Künzel

  3. omics2view.consulting GbR, 24113, Kiel, Germany

    Sven C. Neulinger

Authors
  1. Johannes F. Imhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tanja Rahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sven Künzel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sven C. Neulinger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johannes F. Imhoff.

Ethics declarations

Conflict of interest

All authors declared that they have no potential conflict of interest.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Imhoff, J.F., Rahn, T., Künzel, S. et al. New insights into the metabolic potential of the phototrophic purple bacterium Rhodopila globiformis DSM 161T from its draft genome sequence and evidence for a vanadium-dependent nitrogenase. Arch Microbiol 200, 847–857 (2018). https://doi.org/10.1007/s00203-018-1489-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-018-1489-z

Keywords

Search

Navigation