Complete Genome Sequence of Lactobacillus hilgardii LMG 7934, Carrying the Gene Encoding for the Novel PII-Like Protein PotN.
Journal
Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
19
05
2020
accepted:
07
08
2020
pubmed:
18
8
2020
medline:
15
5
2021
entrez:
18
8
2020
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 32803419
doi: 10.1007/s00284-020-02161-6
pii: 10.1007/s00284-020-02161-6
doi:
Substances chimiques
Bacterial Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3538-3545Subventions
Organisme : Council on grants of the President of the Russian Federation
ID : MD- 572.2020.4
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC 2124
Organisme : Ministry of science and higher education of Russian Federation
ID : 075-02-2020-1478
Références
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
doi: 10.1073/pnas.0607117103
pubmed: 17030793
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
doi: 10.1007/978-1-4615-5817-0_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
doi: 10.1186/1475-2859-10-S1-S5
pubmed: 21995342
pmcid: 3231931
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
doi: 10.5851/kosfa.2016.36.4.499
pubmed: 27621691
pmcid: 5018510
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
doi: 10.1155/2015/625740
pubmed: 25802859
pmcid: 4352725
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
doi: 10.1016/j.mib.2013.06.008
pubmed: 23866974
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
doi: 10.1016/j.fm.2013.10.003
pubmed: 24290648
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
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
doi: 10.1111/febs.14021
pubmed: 28109177
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
doi: 10.1128/JB.181.16.5042-5050.1999
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
doi: 10.1146/annurev.micro.61.080706.093409
pubmed: 17506680
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
doi: 10.1016/j.tim.2007.11.004
pubmed: 18182294
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
doi: 10.1111/j.1574-6976.2012.00351.x
pubmed: 22861350
Merrick M (2015) Post-translational modification of P-II signal transduction proteins. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00763
doi: 10.3389/fmicb.2014.00763
pubmed: 25610437
pmcid: 4285133
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
doi: 10.1038/s41598-017-19046-7
pubmed: 29335634
pmcid: 5768801
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
doi: 10.1111/febs.13584
pubmed: 26527104
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
doi: 10.1371/journal.pone.0137114
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
doi: 10.1016/j.jmb.2014.05.008
pubmed: 24846646
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
doi: 10.1016/s0966-842x(00)01709-1
pubmed: 10754576
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
doi: 10.1074/jbc.M110.153908
pubmed: 20639578
pmcid: 2945594
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
doi: 10.1073/pnas.1007015107
pubmed: 20716687
Andrews S (2010) FastQC: a quality control tool for high throughput sequence data.
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
doi: 10.1371/journal.pcbi.1005595
pubmed: 28594827
pmcid: 5481147
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069. https://doi.org/10.1093/bioinformatics/btu153
doi: 10.1093/bioinformatics/btu153
pubmed: 24642063
pmcid: 24642063
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
doi: 10.1186/1471-2164-9-75
pubmed: 2265698
pmcid: 2265698
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
doi: 10.1186/1471-2105-10-421
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
doi: 10.1074/jbc.M607582200
pubmed: 17001076
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
doi: 10.1111/j.1742-4658.2011.08102.x
pubmed: 21435182
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
doi: 10.1111/j.1365-2958.2008.06514.x
pubmed: 19007411
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
doi: 10.1128/jb.184.15.4081-4088.2002
pubmed: 12107124
pmcid: 135213
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
doi: 10.1128/JB.180.10.2652-2659.1998
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
doi: 10.1128/JB.00613-08
pubmed: 18689479
pmcid: 2566009
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
doi: 10.1016/s0923-2508(01)01197-4
pubmed: 11421273
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
doi: 10.1128/MMBR.00025-13
pubmed: 24296575
pmcid: 3973380
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
doi: 10.1007/BF00027390
pubmed: 24272346
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
doi: 10.1146/annurev.micro.57.030502.090820
pubmed: 12730324
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
doi: 10.1073/pnas.93.17.8841
pubmed: 8799114
Sonenshein AL (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5(12):917–927. https://doi.org/10.1038/nrmicro1772
doi: 10.1038/nrmicro1772
pubmed: 17982469
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
doi: 10.1111/j.1365-2958.2007.05816.x
pubmed: 17608797
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
doi: 10.1046/j.1365-2958.1999.01333.x
pubmed: 10231480
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
doi: 10.1074/jbc.M115.680991
pubmed: 26635369
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
doi: 10.1016/j.febslet.2013.03.015
pubmed: 23535029