Computational and cellular exploration of the protein-protein interaction between Vibrio fischeri STAS domain protein SypA and serine kinase SypE

References

• Nooren IMA, Thornton JM. Diversity of protein–protein interactions. Embo J. 2003;22:3486–15.
   PubMed Web of Science ®Google Scholar
• Moy BE, Seshu J. STAS domain only proteins in bacterial gene regulation. Front Cell Infect Microbiol. 2021;11:564.
   Web of Science ®Google Scholar
• Aravind L, Koonin EV. The STAS domain — a link between anion transporters and antisigma-factor antagonists. Curr Biol. 2000;10:R53–55.
   PubMed Web of Science ®Google Scholar
• Losick R, Pero J. Cascades of sigma factors. Cell. 1981;25:582–584.
   PubMed Web of Science ®Google Scholar
• Campbell EA, Westblade LF, Darst SA. Regulation of bacterial RNA polymerase sigma factor activity: a structural perspective. Curr Opin Microbiol. 2008;11:121–127.
   PubMed Web of Science ®Google Scholar
• Marles-Wright J, Grant T, Delumeau O, et al. Molecular architecture of the “stressosome. A Signal Integration and Transduction Hub. 2008;322:6.
   Google Scholar
• Miksys A, Fu L, Madej MG, et al. Molecular insights into intra-complex signal transmission during stressosome activation. Commun Biol. 2022;5:1–12.
   PubMed Web of Science ®Google Scholar
• Kovacs H, Comfort D, Lord M, et al. Solution structure of SpoIIAA, a phosphorylatable component of the system that regulates transcription factor sigmaF of Bacillus subtilis. Proc Natl Acad Sci U S A. 1998;95:5067–5071.
   PubMed Web of Science ®Google Scholar
• Masuda S, Murakami KS, Wang S, et al. Crystal structures of the ADP and ATP bound forms of the Bacillus anti-sigma factor SpoIIAB in complex with the anti-anti-sigma SpoIIAA. J Mol Biol. 2004;340:941–956.
   PubMed Web of Science ®Google Scholar
• Garsin DA, Paskowitz DM, Duncan L, et al. Evidence for common sites of contact between the antisigma factor SpoIIAB and its partners SpoIIAA and the developmental transcription factor sigmaF in Bacillus subtilis. J Mol Biol. 1998;284:557–568.
   PubMed Web of Science ®Google Scholar
• Seavers PR, Lewis RJ, Brannigan JA, et al. Structure of the Bacillus cell fate determinant SpoIIAA in phosphorylated and unphosphorylated forms. Struct. 1993;9(2001):605–614.
   Google Scholar
• Lee CS, Clarkson J, Shu JC, et al. Bacillus subtilis mutations that alter the pathway of phosphorylation of the anti-anti-sigmaF factor SpoIIAA lead to a Spo- phenotype. Mol Microbiol. 2001;40:9–19.
   PubMed Web of Science ®Google Scholar
• Diederich B, Wilkinson JF, Magnin T, et al. Role of interactions between SpoIIAA and SpoIIAB in regulating cell-specific transcription factor sigma F of Bacillus subtilis. Genes Dev. 1994;8:2653–2663.
   PubMed Web of Science ®Google Scholar
• Schmidt R, Margolis P, Duncan L, et al. Control of developmental transcription factor sigma F by sporulation regulatory proteins SpoIIAA and SpoIIAB in Bacillus subtilis. Proc Natl Acad Sci U S A. 1990;87:9221–9225.
   PubMed Web of Science ®Google Scholar
• Voelker U, Voelker A, Maul B, et al. Separate mechanisms activate sigma B of Bacillus subtilis in response to environmental and metabolic stresses. J Bacteriol. 1995;177:3771–3780.
   PubMed Web of Science ®Google Scholar
• Voelker U, Voelker A, Haldenwang WG. Reactivation of the Bacillus subtilis anti-sigma B antagonist, RsbV, by stress- or starvation-induced phosphatase activities. J Bacteriol. 1996;178:5456–5463.
   PubMed Web of Science ®Google Scholar
• Kozak NA, Mattoo S, Foreman-Wykert AK, et al. Interactions between partner switcher orthologs BtrW and BtrV regulate type III secretion in Bordetella. J Bacteriol. 2005;187:5665–5676.
   PubMed Web of Science ®Google Scholar
• Mercer RG, Lang AS. Identification of a predicted partner-switching system that affects production of the gene transfer agent RcGTA and stationary phase viability in Rhodobacter capsulatus. BMC Microbiol. 2014;14:71.
   PubMed Web of Science ®Google Scholar
• Riley KW, Gonzalez A, Risser DD. A partner-switching regulatory system controls hormogonium development in the filamentous cyanobacterium Nostoc punctiforme. Mol Microbiol. 2018;109:555–569.
   PubMed Web of Science ®Google Scholar
• Morris AR, Visick KL. The response regulator SypE controls biofilm formation and colonization through phosphorylation of the syp-encoded regulator SypA in Vibrio fischeri. Mol Microbiol. 2013;87:509–525.
   PubMed Web of Science ®Google Scholar
• Morris AR, Visick KL. Control of biofilm formation and colonization in Vibrio fischeri: a role for partner switching? Environ Microbiol. 2010;12:2051–2059.
   PubMed Web of Science ®Google Scholar
• Yip ES, Grublesky BT, Hussa EA, et al. A novel, conserved cluster of genes promotes symbiotic colonization and σ54-dependent biofilm formation by Vibrio fischeri. Mol Microbiol. 2005;57:1485–1498.
   PubMed Web of Science ®Google Scholar
• Yip ES, Geszvain K, DeLoney-Marino CR, et al. The symbiosis regulator rscS controls the syp gene locus, biofilm formation and symbiotic aggregation by Vibrio fischeri. Mol Microbiol. 2006;62:1586–1600.
   PubMed Web of Science ®Google Scholar
• Shibata S, Yip ES, Quirke KP, et al. Roles of the structural symbiosis polysaccharide (syp) genes in host colonization, biofilm formation, and polysaccharide biosynthesis in Vibrio fischeri. J Bacteriol. 2012;194:6736–6747.
   PubMed Web of Science ®Google Scholar
• Hussa EA, Darnell CL, Visick KL. RscS functions upstream of SypG to control the syp locus and biofilm formation in Vibrio fischeri. J Bacteriol. 2008;190:4576–4583.
   PubMed Web of Science ®Google Scholar
• Morris AR, Darnell CL, Visick KL. Inactivation of a novel response regulator is necessary for biofilm formation and host colonization by Vibrio fischeri. Mol Microbiol. 2011;82:114–130.
   PubMed Web of Science ®Google Scholar
• Morris AR, Visick KL, Beloin C. Inhibition of SypG-induced biofilms and host colonization by the negative regulator SypE in Vibrio fischeri. PLoS ONE. 2013;8:e60076.
   PubMed Web of Science ®Google Scholar
• Thompson CM, Marsden AE, Tischler AH, et al. Vibrio fischeri biofilm formation prevented by a trio of regulators. Appl Environ Microbiol 2018;84:e01257–18. DOI:10.1128/AEM.01257-18
   PubMed Web of Science ®Google Scholar
• Yildiz FH, Visick KL. Vibrio biofilms: so much the same yet so different. Trends Microbiol. 2009;17:109–118.
   PubMed Web of Science ®Google Scholar
• Bateman A, Martin M-J, Orchard S. The UniProt Consortium, UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res. 2023;51:D523–531.
   PubMed Web of Science ®Google Scholar
• Baek M, DiMaio F, Anishchenko I, et al. Accurate prediction of protein structures and interactions using a three-track neural network. Science. 2021;373:871–876.
   PubMed Web of Science ®Google Scholar
• Mirdita M, Schütze K, Moriwaki Y, et al. ColabFold: making protein folding accessible to all. Nat Methods. 2022;19:679–682.
   PubMed Web of Science ®Google Scholar
• Williams CJ, Headd JJ, Moriarty NW, et al. MolProbity: more and better reference data for improved all-atom structure validation. Protein Sci Publ Protein Soc. 2018;27:293–315.
   PubMed Web of Science ®Google Scholar
• Balbin C, Bliven S, Pymol-color-alphafold, (2022). https://github.com/cbalbin-bio/pymol-color-alphafold
   Google Scholar
• Boettcher KJ, Ruby EG. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J Bacteriol. 1990;172:3701–3706.
   PubMed Web of Science ®Google Scholar
• Le Roux F, Binesse J, Saulnier D, et al. Construction of a Vibrio splendidus mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector. Appl Environ Microbiol. 2007;73:777–784.
   PubMed Web of Science ®Google Scholar
• Graf J, Dunlap PV, Ruby EG. Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J Bacteriol. 1994;176:6986–6991.
   PubMed Web of Science ®Google Scholar
• Visick KL, Hodge-Hanson KM, Tischler AH, et al. Tools for rapid genetic engineering of Vibrio fischeri. Appl Environ Microbiol 2018;84:e00850–18. DOI:10.1128/AEM.00850-18
   PubMed Web of Science ®Google Scholar
• Christensen DG, Tepavčević J, Visick KL. Genetic manipulation of Vibrio fischeri. Curr Protoc Microbiol. 2020;59:e115.
   PubMedGoogle Scholar
• Cohen JJ, Eichinger SJ, Witte DA, et al. Control of competence in Vibrio fischeri. Appl Environ Microbiol 2021;87:e01962–20. DOI:10.1128/AEM.01962-20
   PubMed Web of Science ®Google Scholar
• Brooks JF, Gyllborg MC, Cronin DC, et al. Global discovery of colonization determinants in the squid symbiont Vibrio fischeri. Proc Natl Acad Sci U S A. 2014;111:17284–17289.
   PubMed Web of Science ®Google Scholar
• Stabb EV, Ruby EG. RP4-based plasmids for conjugation between Escherichia coli and members of the vibrionaceae. In Methods Enzymol. Academic Press; 2002. pp. 413–426. DOI:10.1016/S0076-6879(02)58106-4
   Google Scholar
• Ho SN, Hunt HD, Horton RM, et al. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 1989;77:51–59.
   PubMed Web of Science ®Google Scholar
• Jumper J, Evans R, Pritzel A, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;1–11. DOI:10.1038/s41586-021-03819-2
   Google Scholar
• Varadi M, Anyango S, Deshpande M, et al. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 2022;50:D439–444.
   PubMed Web of Science ®Google Scholar
• Pathak D, Jin KS, Tandukar S, et al. Structural insights into the regulation of SigB activity by RsbV and RsbW. IUCrJ. 2020;7:737–747.
   PubMed Web of Science ®Google Scholar
• Challoner-Courtney IJ, Yudkin MD. Molecular and phenotypic characterization of promoter-proximal mutations in the spoIIA locus of Bacillus subtilis. J Bacteriol. 1993;175:5636–5641.
   PubMed Web of Science ®Google Scholar
• Evans R, O’Neill M, Pritzel A, et al. Protein complex prediction with AlphaFold-Multimer. 2022;2021:10.04.463034. DOI:10.1101/2021.10.04.463034
   Google Scholar
• Mirdita M, Steinegger M, Söding J. Mmseqs2 desktop and local web server app for fast, interactive sequence searches. Bioinformatics. 2019;35:2856–2858.
   PubMed Web of Science ®Google Scholar
• Krissinel E, Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr. 2004;60:2256–2268.
   PubMed Web of Science ®Google Scholar
• Campbell EA, Masuda S, Sun JL, et al. Crystal structure of the Bacillus stearothermophilus anti-sigma factor SpoIIAB with the sporulation sigma factor sigmaF. Cell. 2002;108:795–807.
   PubMed Web of Science ®Google Scholar
• Bugge K, Brakti I, Fernandes CB, et al. Interactions by disorder – a matter of context. Front Mol Biosci. 2020 [accessed February 1, 2023];7. https://www.frontiersin.org/articles/10.3389/fmolb.2020.00110
   PubMed Web of Science ®Google Scholar
• Uversky VN. Intrinsic disorder, protein-protein interactions, and disease. Adv Protein Chem Struct Biol. 2018;110:85–121.
   PubMed Web of Science ®Google Scholar
• Thompson CM, Visick KL. Assessing the function of STAS domain protein SypA in Vibrio fischeri using a comparative analysis. Front Microbiol. 2015;6. DOI:10.3389/fmicb.2015.00760
   Web of Science ®Google Scholar
• Koide S, Sidhu SS. The importance of being tyrosine: lessons in molecular recognition from minimalist synthetic binding proteins. ACS Chem Biol. 2009;4:325–334.
   PubMed Web of Science ®Google Scholar
• Jones S, Thornton JM. Principles of protein-protein interactions. Proc Natl Acad Sci U S A. 1996;93:13–20.
   PubMed Web of Science ®Google Scholar
• Conte LL, Chothia C, Janin J, The atomic structure of protein-protein recognition sites11Edited by Fersht AR. The atomic structure of protein-protein recognition sites11Edited by. J Mol Biol. 1999;285:2177–2198.
   PubMed Web of Science ®Google Scholar
• Chen C-C, Lewis RJ, Harris R, et al. A supramolecular complex in the environmental stress signaling pathway of Bacillus subtilis. Mol Microbiol. 2003;49:1657–1669.
   PubMed Web of Science ®Google Scholar
• Akbar S, Gaidenko TA, Kang CM, et al. New family of regulators in the environmental signaling pathway which activates the general stress transcription factor sigma(B) of Bacillus subtilis. J Bacteriol. 2001;183:1329–1338.
   PubMed Web of Science ®Google Scholar
• Heinz V, Jäckel W, Kaltwasser S, et al. The Vibrio vulnificus stressosome is an oxygen-sensor involved in regulating iron metabolism. Commun Biol. 2022;5:1–14.
   PubMed Web of Science ®Google Scholar