Skip to main content

Complete Genome Sequence of Lactobacillus hilgardii LMG 7934, Carrying the Gene Encoding for the Novel PII-Like Protein PotN

Abstract

Lactic acid bacteria are widespread in various ecological niches with the excess of nutrients and have reduced capabilities to adapt to starvation. Among more than 280 Lactobacillus species known to the date, only five, including Lactobacillus hilgardii, carry in their genome the gene encoding for PII-like protein, one of the central regulators of cellular metabolism generally responding to energy- and carbon–nitrogen status in many free-living Bacteria, Archaea and in plant chloroplasts. In contrast to the classical PII encoding genes, in L. hilgardii genome the gene for PII homologue is located within the potABCD operon, encoding the ABC transporter for polyamines. Based on the unique genetic context and low sequence identity with genes of any other so-far characterized PII subfamilies, we termed this gene potN (Pot-protein, Nucleotide-binding). The second specific feature of L. hilgardii genome is that many genes encoding the proteins with similar function are present in two copies, while with low mutual identity. Thus, L. hilgardii LMG 7934 genome carries two genes of glutamine synthetase with 55% identity. One gene is located within classical glnRA operon with the gene of GlnR-like transcriptional regulator, while the second is monocistronic. Together with the relative large genome of L. hilgardii as compared to other Lactobacilli (2.771.862 bp vs ~ 2.2 Mbp in median), these data suggest significant re-arrangements of the genome and a wider range of adaptive capabilities of L. hilgardii in comparison to other bacteria of the genus Lactobacillus.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E et al (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103(42):15611–15616. https://doi.org/10.1073/pnas.0607117103

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hammes WP, Vogel RF (1995) The genus Lactobacillus. In: Wood BJB, Holzapfel WH (eds) The genera of lactic acid bacteria. Springer, Boston, pp 19–54

    Chapter  Google Scholar 

  3. Rhee SJ, Lee JE, Lee CH (2011) Importance of lactic acid bacteria in Asian fermented foods. Microb Cell Fact. 10(Suppl 1):S5. https://doi.org/10.1186/1475-2859-10-S1-S5

    Article  PubMed  PubMed Central  Google Scholar 

  4. Wang D, Liu W, Ren Y, De L, Zhang D, Yang Y et al (2016) Isolation and identification of lactic acid bacteria from traditional dairy products in Baotou and Bayannur of Midwestern Inner Mongolia and q-PCR analysis of predominant species. Korean J Food Sci Anim Resour 36(4):499–507. https://doi.org/10.5851/kosfa.2016.36.4.499

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Franciosi E, Carafa I, Nardin T, Schiavon S, Poznanski E, Cavazza A et al (2015) Biodiversity and γ-aminobutyric acid production by lactic acid bacteria isolated from traditional alpine raw cow's milk cheeses. Biomed Res Int 2015:625740. https://doi.org/10.1155/2015/625740

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Foligné B, Daniel C, Pot B (2013) Probiotics from research to market: the possibilities, risks and challenges. Curr Opin Microbiol 16(3):284–292. https://doi.org/10.1016/j.mib.2013.06.008

    Article  PubMed  Google Scholar 

  7. Solieri L, Bianchi A, Mottolese G, Lemmetti F, Giudici P (2014) Tailoring the probiotic potential of non-starter Lactobacillus strains from ripened Parmigiano Reggiano cheese by in vitro screening and principal component analysis. Food Microbiol 38:240–249. https://doi.org/10.1016/j.fm.2013.10.003

    Article  PubMed  CAS  Google Scholar 

  8. Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman W (2009) Bergey's manual of systematic bacteriology, vol 3, 2nd edn. Springer, New York, pp 465–511

    Google Scholar 

  9. Fernandes GD, Hauf K, Sant'Anna FH, Forchhammer K, Passaglia LMP (2017) Glutamine synthetase stabilizes the binding of GlnR to nitrogen fixation gene operators. FEBS J 284(6):903–918. https://doi.org/10.1111/febs.14021

    Article  PubMed  CAS  Google Scholar 

  10. Hu P, Leighton T, Ishkhanova G, Kustu S (1999) Sensing of nitrogen limitation by Bacillus subtilis: comparison to enteric bacteria. J Bacteriol 181(16):5042–5050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Leigh JA, Dodsworth JA (2007) Nitrogen regulation in Bacteria and Archaea. Annu Rev Microbiol 61:349–377. https://doi.org/10.1146/annurev.micro.61.080706.093409

    Article  PubMed  CAS  Google Scholar 

  12. Forchhammer K (2008) P-II signal transducers: novel functional and structural insights. Trends Microbiol 16(2):65–72. https://doi.org/10.1016/j.tim.2007.11.004

    Article  PubMed  CAS  Google Scholar 

  13. Huergo LF, Chandra G, Merrick M (2013) P(II) signal transduction proteins: nitrogen regulation and beyond. FEMS Microbiol Rev 37(2):251–283. https://doi.org/10.1111/j.1574-6976.2012.00351.x

    Article  PubMed  CAS  Google Scholar 

  14. Merrick M (2015) Post-translational modification of P-II signal transduction proteins. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00763

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lapina T, Selim KA, Forchhammer K, Ermilova E (2018) The PII signaling protein from red algae represents an evolutionary link between cyanobacterial and chloroplastida PII proteins. Sci Rep. https://doi.org/10.1038/s41598-017-19046-7

    Article  PubMed  PubMed Central  Google Scholar 

  16. Forchhammer K, Lüddecke J (2016) Sensory properties of the PII signalling protein family. FEBS J 283(3):425–437. https://doi.org/10.1111/febs.13584

    Article  PubMed  CAS  Google Scholar 

  17. Luddecke J, Forchhammer K (2015) Energy sensing versus 2-oxoglutarate dependent ATPase switch in the control of Synechococcus P-II interaction with its targets NAGK and PipX. PLoS ONE 10(8):9. https://doi.org/10.1371/journal.pone.0137114

    Article  CAS  Google Scholar 

  18. Truan D, Bjelic S, Li XD, Winkler FK (2014) Structure and thermodynamics of effector molecule binding to the nitrogen signal transduction P-II protein GInZ from Azospirillum brasilense. J Mol Biol 426(15):2783–2799. https://doi.org/10.1016/j.jmb.2014.05.008

    Article  PubMed  CAS  Google Scholar 

  19. Ninfa AJ, Atkinson MR (2000) PII signal transduction proteins. Trends Microbiol 8(4):172–179. https://doi.org/10.1016/s0966-842x(00)01709-1

    Article  PubMed  CAS  Google Scholar 

  20. Radchenko MV, Thornton J, Merrick M (2010) Control of AmtB-GlnK complex formation by intracellular levels of ATP, ADP, and 2-oxoglutarate. J Biol Chem 285(40):31037–31045. https://doi.org/10.1074/jbc.M110.153908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Llacer JL, Espinosa J, Castells MA, Contreras A, Forchhammer K, Rubio V (2010) Structural basis for the regulation of NtcA-dependent transcription by proteins PipX and PII. Proc Natl Acad Sci USA 107(35):15397–15402. https://doi.org/10.1073/pnas.1007015107

    Article  PubMed  PubMed Central  Google Scholar 

  22. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data.

  23. Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13(6):e1005595. https://doi.org/10.1371/journal.pcbi.1005595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069. https://doi.org/10.1093/bioinformatics/btu153

    Article  PubMed  CAS  Google Scholar 

  25. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K et al (2009) BLAST+: architecture and applications. BMC Bioinform 10:421. https://doi.org/10.1186/1471-2105-10-421

    Article  CAS  Google Scholar 

  27. Heinrich A, Woyda K, Brauburger K, Meiss G, Detsch C, Stulke J et al (2006) Interaction of the membrane-bound GlnK-AmtB complex with the master regulator of nitrogen metabolism TnrA in Bacillus subtilis. J Biol Chem 281(46):34909–34917. https://doi.org/10.1074/jbc.M607582200

    Article  PubMed  CAS  Google Scholar 

  28. Kayumov A, Heinrich A, Fedorova K, Ilinskaya O, Forchhammer K (2011) Interaction of the general transcription factor TnrA with the PII-like protein GlnK and glutamine synthetase in Bacillus subtilis. FEBS J 278(10):1779–1789. https://doi.org/10.1111/j.1742-4658.2011.08102.x

    Article  PubMed  CAS  Google Scholar 

  29. Tremblay PL, Hallenbeck PC (2009) Of blood, brains and bacteria, the Amt/Rh transporter family: emerging role of Amt as a unique microbial sensor. Mol Microbiol 71(1):12–22. https://doi.org/10.1111/j.1365-2958.2008.06514.x

    Article  PubMed  CAS  Google Scholar 

  30. Yakunin AF, Hallenbeck PC (2002) AmtB is necessary for NH(4)(+)-induced nitrogenase switch-off and ADP-ribosylation in Rhodobacter capsulatus. J Bacteriol 184(15):4081–4088. https://doi.org/10.1128/jb.184.15.4081-4088.2002

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Van Dommelen A, Keijers V, Vanderleyden J, de Zamaroczy M (1998) (Methyl)ammonium transport in the nitrogen-fixing bacterium Azospirillum brasilense. J Bacteriol 180(10):2652–2659

    Article  PubMed  PubMed Central  Google Scholar 

  32. Paz-Yepes J, Merino-Puerto V, Herrero A, Flores E (2008) The Amt gene cluster of the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 190(19):6534–6539. https://doi.org/10.1128/JB.00613-08

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Hosie AH, Poole PS (2001) Bacterial ABC transporters of amino acids. Res Microbiol 152(3–4):259–270. https://doi.org/10.1016/s0923-2508(01)01197-4

    Article  PubMed  CAS  Google Scholar 

  34. Van Heeswijk WC, Westerhoff HV, Boogerd FC (2013) Nitrogen assimilation in Escherichia coli: putting molecular data into a systems perspective. Microbiol Mol Biol Rev 77(4):628–695. https://doi.org/10.1128/MMBR.00025-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Lightfoot DA, Baron AJ, Wootton JC (1988) Expression of the Escherichia coli glutamate dehydrogenase gene in the cyanobacterium Synechococcus PCC6301 causes ammonium tolerance. Plant Mol Biol 11(3):335–344. https://doi.org/10.1007/BF00027390

    Article  PubMed  CAS  Google Scholar 

  36. Reitzer L (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57:155–176. https://doi.org/10.1146/annurev.micro.57.030502.090820

    Article  PubMed  CAS  Google Scholar 

  37. Wray LV, Ferson AE, Rohrer K, Fisher SH (1996) TnrA, a transcription factor required for global nitrogen regulation in Bacillus subtilis. Proc Natl Acad Sci USA 93(17):8841–8845. https://doi.org/10.1073/pnas.93.17.8841

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  38. Sonenshein AL (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5(12):917–927. https://doi.org/10.1038/nrmicro1772

    Article  PubMed  CAS  Google Scholar 

  39. Commichau FM, Herzberg C, Tripal P, Valerius O, Stülke J (2007) A regulatory protein-protein interaction governs glutamate biosynthesis in Bacillus subtilis: the glutamate dehydrogenase RocG moonlights in controlling the transcription factor GltC. Mol Microbiol 65(3):642–654. https://doi.org/10.1111/j.1365-2958.2007.05816.x

    Article  PubMed  CAS  Google Scholar 

  40. Fisher SH (1999) Regulation of nitrogen metabolism in Bacillus subtilis: vive la difference! Mol Microbiol 32(2):223–232. https://doi.org/10.1046/j.1365-2958.1999.01333.x

    Article  PubMed  CAS  Google Scholar 

  41. Hauf K, Kayumov A, Gloge F, Forchhammer K (2016) The molecular basis of TnrA control by glutamine synthetase in Bacillus subtilis. J Biol Chem 291(7):3483–3495. https://doi.org/10.1074/jbc.M115.680991

    Article  PubMed  CAS  Google Scholar 

  42. Fedorova K, Kayumov A, Woyda K, Ilinskaja O, Forchhammer K (2013) Transcription factor TnrA inhibits the biosynthetic activity of glutamine synthetase in Bacillus subtilis. FEBS Lett 587(9):1293–1298. https://doi.org/10.1016/j.febslet.2013.03.015

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported in the form of a grant from the President of the Russian Federation for state support to young Russian scientists—doctors of sciences (MD- 572.2020.4 for AK) and by infrastructural funding from DFG Cluster of Excellence EXC 2124 (Controlling Microbes to Fight Infections) at University Tübingen. This work has been performed in frames of Russian Government Program of Competitive Development of Kazan Federal University. The genome assembly and analysis was performed using the facilities of the Scientific and Educational Mathematical Center of the Volga Federal District (Project No. 075-02-2020-1478).

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization—AK and KF; methodology—GO, NG, DK, ES; investigation—DZ, ZI, GO; formal analysis—DZ, AK and KF; resources—AK and KF; visualization—GO; project administration—AK and KF; supervision—AK and KF; funding acquisition—AK and KF; writing—original draft preparation, review and editing—DZ, AK and KF.

Corresponding author

Correspondence to Airat R. Kayumov.

Ethics declarations

Conflict of interest

Authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhuravleva, D.E., Iskhakova, Z.I., Ozhegov, G.D. et al. Complete Genome Sequence of Lactobacillus hilgardii LMG 7934, Carrying the Gene Encoding for the Novel PII-Like Protein PotN. Curr Microbiol 77, 3538–3545 (2020). https://doi.org/10.1007/s00284-020-02161-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-02161-6