ComFB, a new widespread family of c-di-NMP receptor proteins
Open accessPreprint — published as 10.1073/pnas.2513041122
Abstract
Cyclic dimeric GMP (c-di-GMP) is a widespread bacterial second messenger that controls a variety of cellular functions, including protein and polysaccharide secretion, motility, cell division, cell development, and biofilm formation, and contributes to the virulence of some important bacterial pathogens. While the genes for diguanylate cyclases and c-di-GMP hydrolases (active or mutated) can be easily identified in microbial genomes, the list of c-di-GMP receptor domains is quite limited, and only two of them, PliZ and MshEN, are found across multiple bacterial phyla. Recently, a new c-di-GMP receptor protein, named CdgR or ComFB, has been identified in cyanobacteria and shown to regulate their cell size and, more recently, natural competence. Sequence and structural analysis indicated that CdgR is part of a widespread ComFB protein family, named after the “late competence development protein ComFB” from Bacillus subtilis . This prompted the suggestion that ComFB and ComFB-like proteins could also be c-di-GMP receptors. Indeed, we revealed that ComFB proteins from Gram-positive B. subtilis and Thermoanaerobacter brockii were able to bind c-di-GMP with high-affinity. The ability to bind c-di-GMP was also demonstrated for the ComFB proteins from clinically relevant Gram-negative bacteria Vibrio cholerae and Treponema denticola . These observations indicate that the ComFB family serves as yet another widespread family of bacterial c-di-GMP receptors. Incidentally, some ComFB proteins were also capable of c-di-AMP binding, identifying them as a unique family of c-di-NMP receptor proteins. The overexpression of comFB in B. subtilis, combined with an elevated concentration of c-di-GMP, suppressed motility, attesting to the biological relevance of ComFB as a c-di-GMP binding protein. IMPORTANCE: The cellular content of the bacterial second messenger c-di-GMP is controlled by c-di-GMP synthases (GGDEF domains) and hydrolases (EAL or HD-GYP domains), whose activities, in turn, respond to the signals perceived by their upstream sensory domains. Cyclic-di-GMP transmits the signals to a variety of its targets, which may contain inactivated GGDEF, EAL, or HD-GYP domains, widespread PilZ or MshEN domains, or various lineage-specific c-di-GMP receptors. Many organisms encode multiple GGDEF domains but few c-di-GMP-binding proteins, suggesting the existence of still unidentified c-di-GMP receptors. Here, we demonstrate that the ComFB family proteins, which include the recently characterized cyanobacterial CdgR/ComFB, constitute yet another widespread family of bacterial c-di-NMP receptors. We additionally show that ComFB controls bacillar motility in a c-di-GMP-dependent manner.
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Cites
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764 · see citing works
Varadi, M., Anyango, S., Deshpande, M., Nair, S., Natassia, C., Yordanova, G., Yuan, D., Stroe, O., Wood, G., Laydon, A., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkab1061 · Cited by 7,850 · see citing works
Pfam: The protein families database in 2021
Mistry, J., Chuguransky, S., Williams, L., Qureshi, M., Salazar, G. A., Sonnhammer, E. L. L., Tosatto, S. C. E., Paladin, L., Raj, S., Richardson, L. J., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkaa913 · Cited by 7,452 · see citing works
Potter, S. C., Luciani, A., Eddy, S. R., Park, Y., Lopez, R., & Finn, R. D. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky448 · Cited by 2,607 · see citing works
A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core
Zimmermann, L., Stephens, A., Nam, S.-Z., Rau, D., Kübler, J., Lozajic, M., Gabler, F., Söding, J., Lupas, A. N., & Alva, V. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.12.007 · Cited by 2,522 · see citing works
Self-citationPaysan‐Lafosse, T., Blum, M., Chuguransky, S., Grego, T., Pinto, B. L., Salazar, G. A., Bileschi, M. L., Peer Bork, B., Bridge, A. J., Colwell, L. J., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac993 · Cited by 2,371 · see citing works
Varadi, M., Bertoni, D., Magana, P., Paramval, U., Pidruchna, I., Radhakrishnan, M., Tsenkov, M., Nair, S., Mirdita, M., Yeo, J., et al. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkad1011 · Cited by 2,052 · see citing works
Cyclic di-GMP: the First 25 Years of a Universal Bacterial Second Messenger
Römling, U., Galperin, M. Y., & Gomelsky, M. (2013) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00043-12 · Cited by 1,679 · see citing works
Self-citationThe conserved domain database in 2023
Wang, J., Chitsaz, F., Derbyshire, M. K., Gonzales, N. R., Gwadz, M., Lu, S., Marchler, G. H., Song, J. S., Thanki, N., Yamashita, R. A., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkac1096 · Cited by 1,277 · see citing works
Cyclic di-GMP: second messenger extraordinaire
Jenal, U., Reinders, A., & Lori, C. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.190 · Cited by 1,046 · see citing works
Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid
Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R., Braun, S., de VROOM, E., van der Marel, G. A., BOOM, J. H. V., et al. (1987) · Nature · doi:10.1038/325279a0 · Cited by 1,018 · see citing works
Dali server: structural unification of protein families
Holm, L. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac387 · Cited by 913 · see citing works
COG database update: focus on microbial diversity, model organisms, and widespread pathogens
Galperin, M. Y., Wolf, Y. I., Makarova, K. S., Alvarez, R. V., Landsman, D., & Koonin, E. V. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1018 · Cited by 911 · see citing works
Self-citationProtein Sequence Analysis Using the MPI Bioinformatics Toolkit
Gabler, F., Nam, S., Till, S., Mirdita, M., Steinegger, M., Söding, J., Lupas, A. N., & Alva, V. (2020) · Current Protocols in Bioinformatics · doi:10.1002/cpbi.108 · Cited by 831 · see citing works
Self-citationCLANS: a Java application for visualizing protein families based on pairwise similarity
Frickey, T., & Lupas, A. N. (2004) · Bioinformatics · doi:10.1093/bioinformatics/bth444 · Cited by 721 · see citing works
Riboswitches in Eubacteria Sense the Second Messenger Cyclic Di-GMP
Sudarsan, N., Lee, E. R., Zasha Weinberg, A., Moy, R. H., Kim, J. N., Link, K. H., & Breaker, R. R. (2008) · Science · doi:10.1126/science.1159519 · Cited by 720 · see citing works
Identification of FleQ from Pseudomonas aeruginosa as a c‐di‐GMP‐responsive transcription factor
Hickman, J. W., & Harwood, C. S. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06281.x · Cited by 670 · see citing works
Construction and Analysis of Two Genome-Scale Deletion Libraries for Bacillus subtilis
Koo, B., Kritikos, G., Farelli, J. D., Todor, H., Tong, K., Kimsey, H. H., Wapinski, I. N., Galardini, M., Cabal, A., Peters, J. M., et al. (2017) · Cell Systems · doi:10.1016/j.cels.2016.12.013 · Cited by 584 · see citing works
PilZ domain is part of the bacterial c-di-GMP binding protein
Amikam, D., & Galperin, M. Y. (2005) · Bioinformatics · doi:10.1093/bioinformatics/bti739 · Cited by 536 · see citing works
Self-citationWitte, G., Hartung, S., Büttner, K., & Hopfner, K. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.02.020 · Cited by 429 · see citing works
Waters, C. M., Lu, W., Rabinowitz, J. D., et al. (2008) · Journal of Bacteriology · doi:10.1128/jb.01756-07 · Cited by 426 · see citing works
Davies, B. W., Bogard, R. W., Young, T. S., & Mekalanos, J. J. (2012) · Cell · doi:10.1016/j.cell.2012.01.053 · Cited by 425 · see citing works
Vibrio cholerae VpsT Regulates Matrix Production and Motility by Directly Sensing Cyclic di-GMP
Krasteva, P. V., Fong, J. C. N., Shikuma, N. J., Beyhan, S., Navarro, M. V. A. S., Yildiz, F. H., & Sondermann, H. (2010) · Science · doi:10.1126/science.1181185 · Cited by 400 · see citing works
Cyclic di-AMP: another second messenger enters the fray
Corrigan, R. M., & Gründling, A. (2013) · Nature Reviews Microbiology · doi:10.1038/nrmicro3069 · Cited by 376 · see citing works
Systematic identification of conserved bacterial c-di-AMP receptor proteins
Corrigan, R. M., Campeotto, I., Jeganathan, T., Roelofs, K., Lee, V. T., & Gründling, A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300595110 · Cited by 288 · see citing works
Diversity of Cyclic Di-GMP-Binding Proteins and Mechanisms
Chou, S., & Galperin, M. Y. (2015) · Journal of Bacteriology · doi:10.1128/jb.00333-15 · Cited by 263 · see citing works
Self-citationDiversity and classification of cyclic-oligonucleotide-based anti-phage signalling systems
Millman, A., Melamed, S., Amitai, G., & Sorek, R. (2020) · Nature Microbiology · doi:10.1038/s41564-020-0777-y · Cited by 255 · see citing works
Tschowri, N., Schumacher, M. A., Schlimpert, S., Chinnam, N. B., Findlay, K., Brennan, R. G., & Buttner, M. J. (2014) · Cell · doi:10.1016/j.cell.2014.07.022 · Cited by 252 · see citing works
Get the Message Out: Cyclic-Di-GMP Regulates Multiple Levels of Flagellum-Based Motility
Wolfe, A. J., & Visick, K. L. (2007) · Journal of Bacteriology · doi:10.1128/jb.01418-07 · Cited by 235 · see citing works
Chin, K., Lee, Y.-C., Tu, Z., Chen, C.-H., Tseng, Y., Yang, J., Ryan, R. P., McCarthy, Y., Dow, J. M., Wang, A. H. ‐., et al. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.11.076 · Cited by 195 · see citing works
Matsuyama, B. Y., Krasteva, P. V., Baraquet, C., Harwood, C. S., Sondermann, H., & Navarro, M. V. A. S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1523148113 · Cited by 171 · see citing works
Multiple Roles of c-di-GMP Signaling in Bacterial Pathogenesis
Valentini, M., & Filloux, A. (2019) · Annual Review of Microbiology · doi:10.1146/annurev-micro-020518-115555 · Cited by 170 · see citing works
A Large-scale Protein–protein Interaction Analysis in Synechocystis sp. PCC6803
Sato, S., Shimoda, Y., Muraki, A., Kohara, M., Nakamura, Y., & Tabata, S. (2007) · DNA Research · doi:10.1093/dnares/dsm021 · Cited by 169 · see citing works
Cyclic di-AMP Signaling in Bacteria
Stülke, J., & Krüger, L. (2020) · Annual Review of Microbiology · doi:10.1146/annurev-micro-020518-115943 · Cited by 161 · see citing works
Hisert, K. B., MacCoss, M. J., Shiloh, M. U., Darwin, K. H., Singh, S. M., Jones, R. A., Ehrt, S., Zhang, Z., Gaffney, B. L., Gandotra, S., et al. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04632.x · Cited by 149 · see citing works
The ins and outs of cyclic di-GMP signaling in Vibrio cholerae
Conner, J. G., Zamorano‐Sánchez, D., Park, J. H., et al. (2017) · Current Opinion in Microbiology · doi:10.1016/j.mib.2017.01.002 · Cited by 148 · see citing works
Fang, X. D., Ahmad, I., Blanka, A., et al. (2014) · Molecular Microbiology · doi:10.1111/mmi.12672 · Cited by 141 · see citing works
Self-citationWhitney, J. C. C., Colvin, K. M., Marmont, L. S., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.375378 · Cited by 141 · see citing works
A jack of all trades: the multiple roles of the unique essential second messenger cyclic di‐ AMP
Commichau, F. M., Dickmanns, A., Gundlach, J., Ficner, R., & Stülke, J. (2015) · Molecular Microbiology · doi:10.1111/mmi.13026 · Cited by 134 · see citing works
Nucleotide binding by the widespread high-affinity cyclic di-GMP receptor MshEN domain
Wang, Y., Chin, K., Tu, Z., et al. (2016) · Nature Communications · doi:10.1038/ncomms12481 · Cited by 132 · see citing works
Self-citationEvidence for Cyclic Di-GMP-Mediated Signaling in Bacillus subtilis
Chen, Y., Chai, Y., Guo, J.-H., et al. (2012) · Journal of Bacteriology · doi:10.1128/jb.01092-12 · Cited by 121 · see citing works
Standard protocol for mass photometry experiments
Wu, D., & Piszczek, G. (2021) · European Biophysics Journal · doi:10.1007/s00249-021-01513-9 · Cited by 117 · see citing works
Light‐induced alteration of c‐di‐GMP level controls motility of Synechocystis sp. PCC 6803
Savakis, P., Causmaecker, S. D., Angerer, V., Ruppert, U., Anders, K., Essen, L., & Wilde, A. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08106.x · Cited by 116 · see citing works
Cyclic‐di‐GMP regulation of virulence in bacterial pathogens
Hall, C. L., & Lee, V. T. (2017) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1454 · Cited by 106 · see citing works
Cyclic di-AMP, a second messenger of primary importance: tertiary structures and binding mechanisms
He, J., Yin, W., Galperin, M. Y., & Chou, S. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa112 · Cited by 96 · see citing works
Self-citationGao, X., Mukherjee, S., Matthews, P. M., Hammad, L. A., Kearns, D. B., & Dann, C. E. (2013) · Journal of Bacteriology · doi:10.1128/jb.00373-13 · Cited by 88 · see citing works
Londoño‐Vallejo, A., & Dubnau, D. A. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb01674.x · Cited by 87 · see citing works
Self-citationCBASS to cGAS-STING: The Origins and Mechanisms of Nucleotide Second Messenger Immune Signaling
Slavik, K. M., & Kranzusch, P. J. (2023) · Annual Review of Virology · doi:10.1146/annurev-virology-111821-115636 · Cited by 84 · see citing works
P II -like signaling protein SbtB links cAMP sensing with cyanobacterial inorganic carbon response
Selim, K. A., Haase, F., Hartmann, M. D., Hagemann, M., & Forchhammer, K. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803790115 · Cited by 83 · see citing works
Self-citationc-di-GMP Arms an Anti-σ to Control Progression of Multicellular Differentiation in Streptomyces
Gallagher, K. A., Schumacher, M. A., Bush, M. J., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.11.006 · Cited by 76 · see citing works
Cahill, M. A., Ernst, W. H., Janknecht, R., & Nordheim, A. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)00320-3 · Cited by 69 · see citing works
Nesper, J., Hug, I., Kato, S., Hee, C.-S., Habazettl, J. M., Manfredi, P., Grzesiek, S., Schirmer, T., Emonet, T., & Jenal, U. (2017) · eLife · doi:10.7554/elife.28842 · Cited by 64 · see citing works
Schuergers, N., Ruppert, U., Watanabe, S., Nürnberg, D. J., Lochnit, G., Dienst, D. D., Mullineaux, C. W., & Wilde, A. (2014) · Molecular Microbiology · doi:10.1111/mmi.12595 · Cited by 61 · see citing works
Chatterjee, D., Cooley, R. B., Boyd, C. D., Mehl, R. A., O’Toole, G. A., & Sondermann, H. (2014) · eLife · doi:10.7554/elife.03650 · Cited by 57 · see citing works
MotI (DgrA) acts as a molecular clutch on the flagellar stator protein MotA in Bacillus subtilis
Subramanian, S., Gao, X., Dann, C. E., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716231114 · Cited by 57 · see citing works
Cofactor squelching: Artifact or fact?
Schmidt, S. F., Larsen, B. D., Loft, A., & Mandrup, S. (2016) · BioEssays · doi:10.1002/bies.201600034 · Cited by 56 · see citing works
Kovács, Á. T., Smits, W. K., Mirończuk, A. M., et al. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.01937.x · Cited by 55 · see citing works
The ever-expanding world of bacterial cyclic oligonucleotide second messengers
Yoon, S. H., & Waters, C. M. (2021) · Current Opinion in Microbiology · doi:10.1016/j.mib.2021.01.017 · Cited by 55 · see citing works
Selim, K. A., Haffner, M. C., Burkhardt, M., Mantovani, O., Neumann, N., Albrecht, R., Seifert, R., Krüger, L., Stülke, J., Hartmann, M. D., et al. (2021) · Science Advances · doi:10.1126/sciadv.abk0568 · Cited by 48 · see citing works
Self-citationc-di-GMP inhibits the DNA binding activity of H-NS in Salmonella
Li, S., Liu, Q., Duan, C., Li, J., Sun, H., Xu, L., Yang, Q., Wang, Y., Shen, X., & Zhang, L. (2023) · Nature Communications · doi:10.1038/s41467-023-43442-5 · Cited by 47 · see citing works
Krüger, L., Herzberg, C., Rath, H., Pedreira, T., Ischebeck, T., Poehlein, A., Gundlach, J., Daniel, R., Völker, U., Mäder, U., et al. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009092 · Cited by 45 · see citing works
Functional diversity of c-di-GMP receptors in prokaryotic and eukaryotic systems
Khan, F., Jeong, G., Tabassum, N., et al. (2023) · Cell Communication and Signaling · doi:10.1186/s12964-023-01263-5 · Cited by 44 · see citing works
Structural Conservation and Diversity of PilZ-Related Domains
Galperin, M. Y., & Chou, S. (2019) · Journal of Bacteriology · doi:10.1128/jb.00664-19 · Cited by 42 · see citing works
Self-citationMakarova, K. S., Koonin, E. V., Haselkorn, R., et al. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl096 · Cited by 42 · see citing works
Self-citationJunkermeier, E. H., & Hengge, R. (2021) · mBio · doi:10.1128/mbio.03249-21 · Cited by 41 · see citing works
Discovery and characterization of a Gram-positive Pel polysaccharide biosynthetic gene cluster
Whitfield, G. B., Marmont, L. S., Bundalovic-Torma, C., Razvi, E., Roach, E. J., Khursigara, C. M., Parkinson, J., & Howell, P. L. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008281 · Cited by 39 · see citing works
Mouali, Y. E., Kim, H., Ahmad, I., Brauner, A., Liu, Y., Skurnik, M., Galperin, M. Y., & Römling, U. (2017) · Journal of Bacteriology · doi:10.1128/jb.00179-17 · Cited by 37 · see citing works
Self-citationSelim, K., Lapina, T., Forchhammer, K., & Ermilova, E. (2019) · The FEBS Journal · doi:10.1111/febs.14989 · Cited by 34 · see citing works
Self-citationA c-di-GMP binding effector controls cell size in a cyanobacterium
Zeng, X., Huang, M., Sun, Q.-X., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2221874120 · Cited by 32 · see citing works
A novel Ca2+-binding protein influences photosynthetic electron transport in Anabaena sp. PCC 7120
Walter, J., Selim, K. A., Leganés, F., Fernández‐Piñas, F., Vothknecht, U. C., Forchhammer, K., Aro, E., & Gollan, P. J. (2019) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2019.04.007 · Cited by 30 · see citing works
Self-citationSelim, K. A., Haffner, M. C., Mantovani, O., Albrecht, R., Zhu, H., Hagemann, M., Forchhammer, K., & Hartmann, M. D. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2205882120 · Cited by 30 · see citing works
Self-citationCommichau, F. M., & Stülke, J. (2018) · Journal of Bacteriology · doi:10.1128/jb.00166-18 · Cited by 29 · see citing works
Structure and Multitasking of the c-di-GMP-Sensing Cellulose Secretion Regulator BcsE
Zouhir, S., Abidi, W., Caleechurn, M., & Krasteva, P. V. (2020) · mBio · doi:10.1128/mbio.01303-20 · Cited by 29 · see citing works
SwrD (YlzI) Promotes Swarming in Bacillus subtilis by Increasing Power to Flagellar Motors
Hall, A. N., Subramanian, S., Oshiro, R. T., Canzoneri, A. K., & Kearns, D. B. (2017) · Journal of Bacteriology · doi:10.1128/jb.00529-17 · Cited by 28 · see citing works
Selim, K. A., Haffner, M. C., Watzer, B., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-55495-y · Cited by 28 · see citing works
Self-citationWallner, T., Pedroza, L., Voigt, K., et al. (2020) · Photochemical & Photobiological Sciences · doi:10.1039/c9pp00489k · Cited by 28 · see citing works
Mantovani, O., Reimann, V., Haffner, M. C., Herrmann, F. P., Selim, K. A., Forchhammer, K., Hess, W. R., & Hagemann, M. (2022) · New Phytologist · doi:10.1111/nph.18094 · Cited by 28 · see citing works
Self-citationAll DACs in a Row: Domain Architectures of Bacterial and Archaeal Diadenylate Cyclases
Galperin, M. Y. (2023) · Journal of Bacteriology · doi:10.1128/jb.00023-23 · Cited by 28 · see citing works
Self-citationAngerer, V., Schwenk, P., Wallner, T., et al. (2017) · Microbiology · doi:10.1099/mic.0.000475 · Cited by 26 · see citing works
Functional Analysis of the ComK Protein of Bacillus coagulans
Kovács, Á. T., Eckhardt, T. H., van Kranenburg, R., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053471 · Cited by 25 · see citing works
Control of light-dependent behaviour in cyanobacteria by the second messenger cyclic di-GMP
Enomoto, G., Wallner, T., & Wilde, A. (2023) · microLife · doi:10.1093/femsml/uqad019 · Cited by 24 · see citing works
Ahmed, I., Hahn, J., Henrickson, A., Khaja, F. T., Demeler, B., Dubnau, D., & Neiditch, M. (2022) · Nature Communications · doi:10.1038/s41467-022-35129-0 · Cited by 23 · see citing works
Self-citationSkotnicka, D., Steinchen, W., Szadkowski, D., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15628-8 · Cited by 21 · see citing works
Selim, K. A., Tremiño, L., Marco‐Marín, C., et al. (2020) · FEBS Journal · doi:10.1111/febs.15464 · Cited by 21 · see citing works
Self-citationComFC mediates transport and handling of single-stranded DNA during natural transformation
Damke, P. P., Celma, L., Kondekar, S. M., Guilmi, A. M. D., Marsin, S., Dépagne, J., Veaute, X., Legrand, P., Walbott, H., Vercruyssen, J., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29494-z · Cited by 20 · see citing works
Mantovani, O., Haffner, M. C., Selim, K. A., Hagemann, M., & Forchhammer, K. (2023) · microLife · doi:10.1093/femsml/uqad008 · Cited by 20 · see citing works
Self-citationAcuC, a histone deacetylase, contributes to the pathogenicity of Aeromonas hydrophila
Jiang, Q., Chen, W., Qin, Y., et al. (2017) · MicrobiologyOpen · doi:10.1002/mbo3.468 · Cited by 19 · see citing works
Mazzotta, M. G., McIlvin, M. R., Moran, D. M., et al. (2021) · Metallomics · doi:10.1093/mtomcs/mfab060 · Cited by 19 · see citing works
PII-like signaling proteins: a new paradigm in orchestrating cellular homeostasis
Selim, K. A., & Alva, V. (2024) · Current Opinion in Microbiology · doi:10.1016/j.mib.2024.102453 · Cited by 19 · see citing works
Self-citationStructural characterization of the late competence protein ComFB from Bacillus subtilis
Sysoeva, T. A., Bane, L. B., Xiao, D. Y., et al. (2014) · Bioscience Reports · doi:10.1042/bsr20140174 · Cited by 16 · see citing works
Mantovani, O., Haffner, M. C., Walke, P., Elshereef, A. A., Wagner, B. C., Petras, D., Forchhammer, K., Selim, K. A., & Hagemann, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-58354-7 · Cited by 10 · see citing works
Self-citationNie, L., Xiao, Y., Zhou, T., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad1117 · Cited by 9 · see citing works
Haffner, M. C., Hou, W., Mantovani, O., Walke, P., Hauf, K., Borisova, M., Hagemann, M., Zhou, C., Forchhammer, K., & Selim, K. A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.10.552651 · Cited by 9 · see citing works
Self-citationCaldicellulosiruptor bescii Adheres to Polysaccharides via a Type IV Pilin-Dependent Mechanism
Khan, A., Hauk, V. J., Ibrahim, M., Raffel, T. R., & Blumer‐Schuette, S. E. (2020) · Applied and Environmental Microbiology · doi:10.1128/aem.00200-20 · Cited by 8 · see citing works
The second messenger c-di-AMP controls natural competence via ComFB signaling protein
Samir, S., Doello, S., Enkerlin, A. M., Zimmer, E., Haffner, M. C., Muller, T. A., Dengler, L., Lambidis, S. P., Sivabalasarma, S., Albers, S., et al. (2025) · Cell Discovery · doi:10.1038/s41421-025-00816-x · Cited by 7 · see citing works
Self-citationDiurnal rhythm causes metabolic crises in the cyanobacterial mutants of c-di-AMP signaling cascade
Haffner, M. C., Enkerlin, A. M., Mantovani, O., et al. (2025) · iScience · doi:10.1016/j.isci.2025.113261 · Cited by 6 · see citing works
Self-citation
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The second messenger c-di-AMP controls natural competence via ComFB signaling protein
Samir, S., Doello, S., Enkerlin, A. M., Zimmer, E., Haffner, M. C., Muller, T. A., Dengler, L., Lambidis, S. P., Sivabalasarma, S., Albers, S., et al. (2025) · Cell Discovery · doi:10.1038/s41421-025-00816-x · Cited by 7 · see citing works
Self-citationDiurnal rhythm causes metabolic crises in the cyanobacterial mutants of c-di-AMP signaling cascade
Haffner, M. C., Enkerlin, A. M., Mantovani, O., et al. (2025) · iScience · doi:10.1016/j.isci.2025.113261 · Cited by 6 · see citing works
Self-citationWallner, T., He, C., Samir, S., et al. (2026) · Microbiological Research · doi:10.1016/j.micres.2026.128607 · Cited by 3 · see citing works
Self-citationZimmer, E., Poppitz, C., Klähn, S., & Selim, K. A. (2026) · The Plant Journal · doi:10.1111/tpj.70974 · Cited by 2 · see citing works
Self-citationHiguera‐Llantén, S., Ojeda, N., Protz, J., et al. (2026) · Microbiology Spectrum · doi:10.1128/spectrum.03173-25 · Cited by 1 · see citing works
ComFB bound to c-di-GMP reduces swimming speed and tumbling frequency in B. subtilisPreprint
Hahn, J., Noland, R., Celma, L., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.11.664319 · Cited by 1 · see citing works
Self-citationThe calcium-binding protein CSE links Ca2+ signaling with cell-cell communication in cyanobacteria
Muller, T. A., Stahlecker, F., Roganowicz, K., et al. (2026) · The EMBO Journal · doi:10.1038/s44318-026-00893-y
Self-citation
- Authors
- Samir, S., Elshereef, A. A., Alva, V., Hahn, J., Dubnau, D., Galperin, M. Y., & Selim, K. A.
- Affiliations
- Ain Shams University (EG)
- National Research Centre (EG)
- Max Planck Institute for Biology (DE)
- Rutgers, The State University of New Jersey (US)
- National Institutes of Health (US)
- Heinrich Heine University Düsseldorf (DE)
- Corresponding author
- Selim, Khaled A.
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- openRxiv
- Published
- 2024-11-10
- Volume
- 122
- Issue
- 38
- Pages
- e2513041122-e2513041122
- ISSN
- 0027-8424 (ISSN-L)
- PMC
- PMC11581024
- OpenAlex
- W4414322116
- Cited by
- 7
- References
- 98
- Citations by year
- 2026: 4 · 2025: 3
- FWCI
- 2.11
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (submittedVersion, cc-by-nc-nd)
- Universitätsbibliothek Tübingen
- Funders
- Deutsche Forschungsgemeinschaft (SFB1381, SE 3449/3‐1, SPP 2389, EXC 2124, 390838134, 403222702)
- Huazhong Agricultural University
- Norsk Romsenter
- National Institutes of Health (Z01 LM000061)
- National Institute of General Medical Sciences (R15GM123487, R01GM057720)
- U.S. National Library of Medicine (Z01LM000073)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Phosphodiesterase function and regulation
- Keywords
- c-di-GMP, c-di-AMP, bacterial second messenger, bacterial motility, natural competence, cell size control, Bacillus subtilis, Shewanella oneidensis, Vibrio cholerae, Treponema denticola, Thermoanaerobacter brockii, protein evolution
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