Atypical cyclic di-AMP signaling is essential for Porphyromonas gingivalis growth and regulation of cell envelope homeostasis and virulence

  • Hajishengallis, G. & Lamont, R. J. Past the pink complicated and into extra complexity: the polymicrobial synergy and dysbiosis (PSD) mannequin of periodontal illness etiology. Mol. Oral. Microbiol. 27, 409–419 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Lamont, R. J., Koo, H. & Hajishengallis, G. The oral microbiota: dynamic communities and host interactions. Nat. Rev. Microbiol. 16, 745–759 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Weinberg, A., Belton, C. M., Park, Y. & Lamont, R. J. Function of fimbriae in Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 65, 313–316 (1997).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Potempa, J., Banbula, A. & Travis, J. Function of bacterial proteinases in matrix destruction and modulation of host responses. Periodontol 2000 24, 153–192 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Socransky, S. S., Haffajee, A. D., Smith, C. & Dibart, S. Relation of counts of microbial species to scientific standing on the sampled website. J. Clin. Periodontol. 18, 766–775 (1991).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Uematsu, H. & Hoshino, E. Predominant obligate anaerobes in human periodontal pockets. J. Periodontal Res 27, 15–19 (1992).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Mysak, J. et al. Porphyromonas gingivalis: main periodontopathic pathogen overview. J. Immunol. Res 2014, 476068 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Cugini, C., Klepac-Ceraj, V., Rackaityte, E., Riggs, J. E. & Davey, M. E. Porphyromonas gingivalis: retaining the pathos out of the biont. J. Oral Microbiol. 5, 19804 (2013).

  • How, Okay. Y., Music, Okay. P. & Chan, Okay. G. Porphyromonas gingivalis: an outline of periodontopathic pathogen beneath the gum line. Entrance. Microbiol. 7, 53 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Olsen, I., Lambris, J. D. & Hajishengallis, G. Porphyromonas gingivalis disturbs host-commensal homeostasis by altering complement perform. J. Oral. Microbiol. 9, 1340085 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Lamont, R. J. & Jenkinson, H. F. Life beneath the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62, 1244–1263 (1998).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Hajishengallis, G. & Lamont, R. J. Breaking unhealthy: manipulation of the host response by Porphyromonas gingivalis. Eur. J. Immunol. 44, 328–338 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Guo, Y., Nguyen, Okay. A. & Potempa, J. Dichotomy of gingipains motion as virulence elements: from cleaving substrates with the precision of a surgeon’s knife to a meat chopper-like brutal degradation of proteins. Periodontol 2000 54, 15–44 (2010).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Grenier, D. et al. Impact of inactivation of the Arg- and/or Lys-gingipain gene on chosen virulence and physiological properties of Porphyromonas gingivalis. Infect. Immun. 71, 4742–4748 (2003).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Slaney, J. M., Gallagher, A., Aduse-Opoku, J., Pell, Okay. & Curtis, M. A. Mechanisms of resistance of Porphyromonas gingivalis to killing by serum complement. Infect. Immun. 74, 5352–5361 (2006).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Moradali, M. F. & Davey, M. E. Metabolic plasticity permits way of life transitions of Porphyromonas gingivalis npj Biofilms Microbiomes 7, 1–13 (2021).

  • Moradali, M. F., Ghods, S., Angelini, T. E. & Davey, M. E. Amino acids as wetting brokers: floor translocation by Porphyromonas gingivalis. ISME J. 13, 1560–1574 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Gürsoy, U. Okay., Gürsoy, M., Könönen, E. & Sintim, H. O. Cyclic dinucleotides in oral micro organism and in oral biofilms. Entrance. Cell Infect. Microbiol 7, 273 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Nelson, J. W. et al. Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat. Chem. Biol. 9, 834–839 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Stülke, J. & Krüger, L. Cyclic di-AMP signaling in micro organism. Annu. Rev. Microbiol 74, 159–179 (2020).

    PubMed 
    Article 

    Google Scholar
     

  • Yin, W. et al. A decade of analysis on the second messenger c-di-AMP. FEMS Microbiol Rev. 44, 701–724 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Chaudhuri, S. et al. Identification of a diguanylate cyclase and its position in Porphyromonas gingivalis virulence. Infect. Immun. 82, 2728–2735 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Römling, U., Galperin, M. Y. & Gomelsky, M. Cyclic di-GMP: the primary 25 years of a common bacterial second messenger. Microbiol. Mol. Biol. Rev. 77, 1–52 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Pesavento, C. & Hengge, R. Bacterial nucleotide-based second messengers. Curr. Opin. Microbiol. 12, 170–176 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Enersen, M., Olsen, I., Kvalheim, Ø. & Caugant, D. A. fimA genotypes and multilocus sequence sorts of Porphyromonas gingivalis from sufferers with periodontitis. J. Clin. Microbiol. 46, 31–42 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Igboin, C. O., Griffen, A. L. & Leys, E. J. Porphyromonas gingivalis pressure range. J. Clin. Microbiol. 47, 3073–3081 (2009).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Chastain-Gross, R. P. et al. Genome Sequence of Porphyromonas gingivalis Pressure 381. Genome Announc 5, e01467-16 (2017).

  • Rodrigues, P. H. et al. Porphyromonas gingivalis pressure particular interactions with human coronary artery endothelial cells: a comparative examine. PLoS ONE 7, e52606 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Wang, F. et al. Structural and biochemical characterization of the catalytic domains of GdpP reveals a unified hydrolysis mechanism for the DHH/DHHA1 phosphodiesterase. Biochem J. 475, 191–205 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Commichau, F. M., Heidemann, J. L., Ficner, R. & Stülke, J. Making and breaking of a vital poison: the cyclases and phosphodiesterases that produce and degrade the important second messenger cyclic di-AMP in micro organism. J. Bacteriol. 201, e00462-18 (2019).

  • Hengge, R. et al. Latest advances and present developments in nucleotide second messenger signaling in micro organism. J. Mol. Biol. 431, 908–927 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • He, J., Yin, W., Galperin, M. Y. & Chou, S. H. Cyclic di-AMP, a second messenger of main significance: tertiary buildings and binding mechanisms. Nucleic Acids Res. 48, 2807–2829 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. The Phyre2 internet portal for protein modeling, prediction and evaluation. Nat. Protoc. 10, 845–858 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Fahmi, T., Port, G. C. & Cho, Okay. H. c-di-AMP: a vital molecule within the signaling pathways that regulate the viability and virulence of Gram-positive micro organism. Genes 8, 197 (2017).

  • Hutcherson, J. A. et al. Comparability of inherently important genes of Porphyromonas gingivalis recognized in two transposon-sequencing libraries. Mol. Oral. Microbiol. 31, 354–364 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Klein, B. A., Duncan, M. J. & Hu, L. T. Defining important genes and figuring out virulence elements of Porphyromonas gingivalis by massively parallel sequencing of transposon libraries (Tn-seq). Strategies Mol. Biol. 1279, 25–43 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Klein, B. A. et al. Identification of important genes of the periodontal pathogen Porphyromonas gingivalis. BMC Genomics 13, 578 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Szklarczyk, D. et al. STRING v11: protein-protein affiliation networks with elevated protection, supporting practical discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, D607–D613 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Vermilyea, D. M., Moradali, M. F., Kim, H. M. & Davey, M. E. PPAD exercise promotes outer membrane vesicle biogenesis and floor translocation by Porphyromonas gingivalis. J. Bacteriol. 203, e00343–20 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Loesche, W. J. & Grossman, N. S. Periodontal illness as a selected, albeit continual, an infection: prognosis and therapy. Clin. Microbiol. Rev. 14, 727–752 (2001).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Aduse-Opoku, J. et al. Identification and characterization of the capsular polysaccharide (Okay-antigen) locus of Porphyromonas gingivalis. Infect. Immun. 74, 449–460 (2006).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Chen, T. et al. Comparative whole-genome evaluation of virulent and avirulent strains of Porphyromonas gingivalis. J. Bacteriol. 186, 5473–5479 (2004).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Graham, L. L., Harris, R., Villiger, W. & Beveridge, T. J. Freeze-substitution of gram-negative eubacteria: normal cell morphology and envelope profiles. J. Bacteriol. 173, 1623–1633 (1991).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Tamaki, S., Sato, T. & Matsuhashi, M. Function of lipopolysaccharides in antibiotic resistance and bacteriophage adsorption of Escherichia coli Okay-12. J. Bacteriol. 105, 968–975 (1971).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Rajagopal, S., Sudarsan, N. & Nickerson, Okay. W. Sodium dodecyl sulfate hypersensitivity of clpP and clpB mutants of Escherichia coli. Appl. Environ. Microbiol. 68, 4117–4121 (2002).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Li, Y. et al. LPS transforming is an advanced survival technique for micro organism. Proc. Natl Acad. Sci. USA 109, 8716–8721 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Paramonov, N. et al. Structural evaluation of a novel anionic polysaccharide from Porphyromonas gingivalis pressure W50 associated to Arg-gingipain glycans. Mol. Microbiol. 58, 847–863 (2005).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Rangarajan, M. et al. Identification of a second lipopolysaccharide in Porphyromonas gingivalis W50. J. Bacteriol. 190, 2920–2932 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Veillard, F., Potempa, B., Poreba, M., Drag, M. & Potempa, J. Gingipain aminopeptidase actions in Porphyromonas gingivalis. Biol. Chem. 393, 1471–1476 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Pereira, M. F., Rossi, C. C., da Silva, G. C., Rosa, J. N. & Bazzolli, D. M. S. Galleria mellonella as an an infection mannequin: an in-depth have a look at why it really works and sensible concerns for profitable utility. Pathog. Dis. 78, ftaa056 (2020).

  • Kim, H. M. & Davey, M. E. Synthesis of ppGpp impacts kind IX secretion and biofilm matrix formation in Porphyromonas gingivalis. npj Biofilms Microbiomes 6, 5 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Dos Santos, J. D. et al. Immunomodulatory impact of photodynamic remedy in Galleria mellonella contaminated with Porphyromonas gingivalis. Micro. Pathog. 110, 507–511 (2017).

    Article 

    Google Scholar
     

  • Devaux, L. et al. Cyclic di-AMP regulation of osmotic homeostasis is important in Group B Streptococcus. PLoS Genet. 14, e1007342 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Bai, Y. et al. Mycobacterium tuberculosis Rv3586 (DacA) is a diadenylate cyclase that converts ATP or ADP into c-di-AMP. PLoS ONE 7, e35206 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Corrigan, R. M., Abbott, J. C., Burhenne, H., Kaever, V. & Gründling, A. c-di-AMP is a brand new second messenger in Staphylococcus aureus with a job in controlling cell dimension and envelope stress. PLoS Pathog. 7, e1002217 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Dengler, V. et al. Mutation within the C-di-AMP cyclase dacA impacts health and resistance of methicillin resistant Staphylococcus aureus. PLoS ONE 8, e73512 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Gundlach, J. et al. An important poison: synthesis and degradation of cyclic di-AMP in Bacillus subtilis. J. Bacteriol. 197, 3265–3274 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Luo, Y. & Helmann, J. D. Evaluation of the position of Bacillus subtilis σ(M) in β-lactam resistance reveals a vital position for c-di-AMP in peptidoglycan homeostasis. Mol. Microbiol. 83, 623–639 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Mehne, F. M. et al. Cyclic di-AMP homeostasis in Bacillus subtilis: each lack and excessive degree accumulation of the nucleotide are detrimental for cell development. J. Biol. Chem. 288, 2004–2017 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Oppenheimer-Shaanan, Y., Wexselblatt, E., Katzhendler, J., Yavin, E. & Ben-Yehuda, S. C-di-AMP experiences DNA integrity throughout sporulation in Bacillus subtilis. EMBO Rep. 12, 594–601 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Peng, X., Zhang, Y., Bai, G., Zhou, X. & Wu, H. Cyclic di-AMP mediates biofilm formation. Mol. Microbiol 99, 945–959 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Gao, A. & Serganov, A. Structural insights into recognition of c-di-AMP by the ydaO riboswitch. Nat. Chem. Biol. 10, 787–792 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Krüger, L. et al. A meet-up of two second messengers: the c-di-AMP receptor DarB controls (p)ppGpp synthesis in Bacillus subtilis. Nat. Commun. 12, 1210 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Corrigan, R. M. & Gründling, A. Cyclic di-AMP: one other second messenger enters the fray. Nat. Rev. Microbiol. 11, 513–524 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Zhu, Y. et al. Cyclic-di-AMP synthesis by the diadenylate cyclase CdaA is modulated by the peptidoglycan biosynthesis enzyme GlmM in Lactococcus lactis. Mol. Microbiol. 99, 1015–1027 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Rismondo, J. et al. Phenotypes related to the important diadenylate cyclase CdaA and its potential regulator CdaR within the human pathogen Listeria monocytogenes. J. Bacteriol. 198, 416–426 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Witte, C. E. et al. Cyclic di-AMP is crucial for Listeria monocytogenes development, cell wall homeostasis, and institution of an infection. mBio 4, e00282–13 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Zhang, Z., Liu, D., Liu, S., Zhang, S. & Pan, Y. The position of Porphyromonas gingivalis outer membrane vesicles in periodontal illness and associated systemic ailments. Entrance. Cell Infect. Microbiol. 10, 585917 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Farrugia, C., Stafford, G. P. & Murdoch, C. Porphyromonas gingivalis outer membrane vesicles improve vascular permeability. J. Dent. Res. 99, 1494–1501 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Kuboniwa, M. et al. Streptococcus gordonii makes use of a number of distinct gene capabilities to recruit Porphyromonas gingivalis right into a combined group. Mol. Microbiol. 60, 121–139 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Kuboniwa, M. et al. Metabolic crosstalk regulates Porphyromonas gingivalis colonization and virulence throughout oral polymicrobial an infection. Nat. Microbiol. 2, 1493–1499 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Hajishengallis, G. & Lamont, R. J. Dancing with the celebs: how choreographed bacterial interactions dictate nososymbiocity and provides rise to keystone pathogens, accent pathogens, and pathobionts. Traits Microbiol. 24, 477–489 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Daep, C. A., Novak, E. A., Lamont, R. J. & Demuth, D. R. Structural dissection and in vivo effectiveness of a peptide inhibitor of Porphyromonas gingivalis adherence to Streptococcus gordonii. Infect. Immun. 79, 67–74 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Hausmann, E., Weinfeld, N. & Miller, W. A. Results of lipopolysaccharides on bone resorption in tissue tradition. Calcif. Tissue Res. 9, 272–282 (1972).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Millar, S. J., Goldstein, E. G., Levine, M. J. & Hausmann, E. Modulation of bone metabolism by two chemically distinct lipopolysaccharide fractions from Bacteroides gingivalis. Infect. Immun. 51, 302–306 (1986).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Steffen, M. J., Holt, S. C. & Ebersole, J. L. Porphyromonas gingivalis induction of mediator and cytokine secretion by human gingival fibroblasts. Oral. Microbiol. Immunol. 15, 172–180 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Al-Qutub, M. N. et al. Hemin-dependent modulation of the lipid A construction of Porphyromonas gingivalis lipopolysaccharide. Infect. Immun. 74, 4474–4485 (2006).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Olsen, I. & Singhrao, S. Okay. Significance of heterogeneity in Porhyromonas gingivalis lipopolysaccharide lipid A in tissue particular inflammatory signalling. J. Oral. Microbiol. 10, 1440128 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Matsuura, M. Structural modifications of bacterial lipopolysaccharide that facilitate Gram-Adverse micro organism evasion of host innate immunity. Entrance. Immunol. 4, 109 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Mazgaeen, L. & Gurung, P. Latest advances in lipopolysaccharide recognition methods. Int. J. Mol. Sci. 21, 379 (2020).

  • Moradali, M. F. & Rehm, B. H. A. Polymers produced by micro organism: from pathogenesis to superior supplies. Nat. Rev. Microbiol. 18, 195–210 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Wang, Q., Wright, C. J., Dingming, H., Uriarte, S. M. & Lamont, R. J. Oral group interactions of Filifactor alocis in vitro. PLoS ONE 8, e76271 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Moye, Z. D., Valiuskyte, Okay., Dewhirst, F. E., Nichols, F. C. & Davey, M. E. Synthesis of sphingolipids impacts survival of Porphyromonas gingivalis and the presentation of floor polysaccharides. Entrance. Microbiol. 7, 1919 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Davey, M. E. & Duncan, M. J. Enhanced biofilm formation and lack of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis. J. Bacteriol. 188, 5510–5523 (2006).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Valentine, P. J., Shoemaker, N. B. & Salyers, A. A. Mobilization of bacteroides plasmids by bacteroides conjugal parts. J. Bacteriol. 170, 1319–1324 (1988).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Bähre, H. & Kaever, V. Mass spectrometric evaluation of non-canonical cyclic nucleotides. Handb. Exp. Pharm. 238, 293–306 (2017).

    Article 

    Google Scholar
     

  • Bähre, H. & Kaever, V. Measurement of two’,3’-cyclic nucleotides by liquid chromatography-tandem mass spectrometry in cells. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 964, 208–211 (2014).

    Article 

    Google Scholar
     

  • Beste, Okay. Y., Burhenne, H., Kaever, V., Stasch, J. P. & Seifert, R. Nucleotidyl cyclase exercise of soluble guanylyl cyclase α1β1. Biochemistry 51, 194–204 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • Bähre, H. & Kaever, V. Identification and quantification of cyclic di-guanosine monophosphate and its linear metabolites by reversed-phase LC-MS/MS. Strategies Mol. Biol. 1657, 45–58 (2017).

    PubMed 
    Article 

    Google Scholar
     

  • Bainbridge, B. W., Hirano, T., Grieshaber, N. & Davey, M. E. Deletion of a 77-base-pair inverted repeat aspect alters the synthesis of floor polysaccharides in Porphyromonas gingivalis. J. Bacteriol. 197, 1208–1220 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Gaca, A. O., Abranches, J., Kajfasz, J. Okay. & Lemos, J. A. World transcriptional evaluation of the stringent response in Enterococcus faecalis. Microbiology 158, 1994–2004 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • Comments

    0 comments

    Leave a comment

    Your email address will not be published. Required fields are marked *