دورية أكاديمية

Rhs NADase effectors and their immunity proteins are exchangeable mediators of inter-bacterial competition in Serratia.

التفاصيل البيبلوغرافية
العنوان: Rhs NADase effectors and their immunity proteins are exchangeable mediators of inter-bacterial competition in Serratia.
المؤلفون: Hagan M; School of Life Sciences, University of Dundee, Dow Street, Dundee, DD1 5EH, UK., Pankov G; School of Life Sciences, University of Dundee, Dow Street, Dundee, DD1 5EH, UK., Gallegos-Monterrosa R; School of Life Sciences, University of Dundee, Dow Street, Dundee, DD1 5EH, UK., Williams DJ; School of Life Sciences, University of Dundee, Dow Street, Dundee, DD1 5EH, UK., Earl C; School of Life Sciences, University of Dundee, Dow Street, Dundee, DD1 5EH, UK., Buchanan G; School of Life Sciences, University of Dundee, Dow Street, Dundee, DD1 5EH, UK., Hunter WN; School of Life Sciences, University of Dundee, Dow Street, Dundee, DD1 5EH, UK. w.n.hunter@dundee.ac.uk., Coulthurst SJ; School of Life Sciences, University of Dundee, Dow Street, Dundee, DD1 5EH, UK. s.j.coulthurst@dundee.ac.uk.
المصدر: Nature communications [Nat Commun] 2023 Sep 28; Vol. 14 (1), pp. 6061. Date of Electronic Publication: 2023 Sep 28.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : Nature Pub. Group
مواضيع طبية MeSH: Serratia*/genetics , Type VI Secretion Systems*/genetics , Type VI Secretion Systems*/metabolism, NAD+ Nucleosidase/genetics ; NAD+ Nucleosidase/metabolism ; Bacterial Proteins/metabolism ; Serratia marcescens/metabolism
مستخلص: Many bacterial species use Type VI secretion systems (T6SSs) to deliver anti-bacterial effector proteins into neighbouring bacterial cells, representing an important mechanism of inter-bacterial competition. Specific immunity proteins protect bacteria from the toxic action of their own effectors, whilst orphan immunity proteins without a cognate effector may provide protection against incoming effectors from non-self competitors. T6SS-dependent Rhs effectors contain a variable C-terminal toxin domain (CT), with the cognate immunity protein encoded immediately downstream of the effector. Here, we demonstrate that Rhs1 effectors from two strains of Serratia marcescens, the model strain Db10 and clinical isolate SJC1036, possess distinct CTs which both display NAD(P) + glycohydrolase activity but belong to different subgroups of NADase from each other and other T6SS-associated NADases. Comparative structural analysis identifies conserved functions required for NADase activity and reveals that unrelated NADase immunity proteins utilise a common mechanism of effector inhibition. By replicating a natural recombination event, we show successful functional exchange of CTs and demonstrate that Db10 encodes an orphan immunity protein which provides protection against T6SS-delivered SJC1036 NADase. Our findings highlight the flexible use of Rhs effectors and orphan immunity proteins during inter-strain competition and the repeated adoption of NADase toxins as weapons against bacterial cells.
(© 2023. Springer Nature Limited.)
References: Coulthurst, S. The Type VI secretion system: a versatile bacterial weapon. Microbiology 165, 503–515 (2019). (PMID: 30893029)
Jurenas, D. & Journet, L. Activity, delivery, and diversity of Type VI secretion effectors. Mol. Microbiol. 115, 383–394 (2021). (PMID: 33217073)
Wang, J., Brodmann, M. & Basler, M. Assembly and Subcellular Localization of Bacterial Type VI Secretion Systems. Annu Rev. Microbiol. 73, 621–638 (2019). (PMID: 31226022)
Gallegos-Monterrosa, R. & Coulthurst, S. J. The ecological impact of a bacterial weapon: microbial interactions and the Type VI secretion system. FEMS Microbiol. Rev. 45, fuab033 (2021). (PMID: 341560818632748)
de Moraes, M. H. et al. An interbacterial DNA deaminase toxin directly mutagenizes surviving target populations. eLife 10, e62967 (2021). (PMID: 334482647901873)
Whitney, J. C. et al. An interbacterial NAD(P) + glycohydrolase toxin requires elongation factor Tu for delivery to target cells. Cell 163, 607–619 (2015). (PMID: 264561134624332)
Tang, J. Y., Bullen, N. P., Ahmad, S. & Whitney, J. C. Diverse NADase effector families mediate interbacterial antagonism via the type VI secretion system. J. Biol. Chem. 293, 1504–1514 (2018). (PMID: 29237732)
Sun, J. et al. The tuberculosis necrotizing toxin kills macrophages by hydrolyzing NAD. Nat. Struct. Mol. Biol. 22, 672–678 (2015). (PMID: 262375114560639)
Kirchberger, P. C., Unterweger, D., Provenzano, D., Pukatzki, S. & Boucher, Y. Sequential displacement of Type VI Secretion System effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae. Sci. Rep. 7, 45133 (2017). (PMID: 283276415361080)
Ross, B. D. et al. Human gut bacteria contain acquired interbacterial defence systems. Nature 575, 224–228 (2019). (PMID: 316666996938237)
Jurenas, D. et al. Mounting, structure and autocleavage of a type VI secretion-associated Rhs polymorphic toxin. Nat. Commun. 12, 6998 (2021). (PMID: 348533178636562)
Ahmad, S. et al. Structural basis for effector transmembrane domain recognition by type VI secretion system chaperones. eLife 9, e62816 (2020). (PMID: 333200897773334)
Mahlen, S. D. Serratia infections: from military experiments to current practice. Clin. Microbiol. Rev. 24, 755–791 (2011). (PMID: 219766083194826)
Cianfanelli, F. R. et al. VgrG and PAAR Proteins Define Distinct Versions of a Functional Type VI Secretion System. PLoS Pathog. 12, e1005735 (2016). (PMID: 273520364924876)
Trunk, K. et al. The type VI secretion system deploys antifungal effectors against microbial competitors. Nat. Microbiol. 3, 920–931 (2018). (PMID: 300383076071859)
Alcoforado Diniz, J. & Coulthurst, S. J. Intraspecies Competition in Serratia marcescens Is Mediated by Type VI-Secreted Rhs Effectors and a Conserved Effector-Associated Accessory Protein. J. Bacteriol. 197, 2350–2360 (2015). (PMID: 259398314524185)
Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797 (2007). (PMID: 17681537)
Stromland, O. et al. Discovery of fungal surface NADases predominantly present in pathogenic species. Nat. Commun. 12, 1631 (2021). (PMID: 337125857955114)
Williams, D. J. et al. The genus Serratia revisited by genomics. Nat. Commun. 13, 5195 (2022). (PMID: 360576399440931)
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021). (PMID: 342658448371605)
Murdoch, S. L. et al. The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J. Bacteriol. 193, 6057–6069 (2011). (PMID: 218907053194891)
Donato, S. L. et al. The beta-encapsulation cage of rearrangement hotspot (Rhs) effectors is required for type VI secretion. Proc. Natl Acad. Sci. USA 117, 33540–33548 (2020). (PMID: 333234877777165)
Tak, U. et al. The tuberculosis necrotizing toxin is an NAD + and NADP + glycohydrolase with distinct enzymatic properties. J. Biol. Chem. 294, 3024–3036 (2019). (PMID: 30593509)
Whitney, J. C. et al. A broadly distributed toxin family mediates contact-dependent antagonism between gram-positive bacteria. eLife 6, e26938 (2017). (PMID: 286962035555719)
Carobbi, A. et al. An antibacterial T6SS in Pantoea agglomerans pv. betae delivers a lysozyme-like effector to antagonize competitors. Environ. Microbiol. 24, 4787–4802 (2022). (PMID: 357061359796082)
Amjad, S. et al. Role of NAD + in regulating cellular and metabolic signaling pathways. Mol. Metab. 49, 101195 (2021). (PMID: 336097667973386)
Canto, C., Menzies, K. J. & Auwerx, J. NAD + Metabolism and the Control of Energy Homeostasis: A Balancing Act between Mitochondria and the Nucleus. Cell Metab. 22, 31–53 (2015). (PMID: 261189274487780)
Ma, J. et al. The Hcp proteins fused with diverse extended-toxin domains represent a novel pattern of antibacterial effectors in type VI secretion systems. Virulence 8, 1189–1202 (2017). (PMID: 280605745711352)
Salomon, D., Gonzalez, H., Updegraff, B. L. & Orth, K. Vibrio parahaemolyticus type VI secretion system 1 is activated in marine conditions to target bacteria, and is differentially regulated from system 2. PloS One 8, e61086 (2013). (PMID: 236137913628861)
LaCourse, K. D. et al. Conditional toxicity and synergy drive diversity among antibacterial effectors. Nat. Microbiol. 3, 440–446 (2018). (PMID: 294597335876133)
Garb, J. et al. Multiple phage resistance systems inhibit infection via SIR2-dependent NAD + depletion. Nat. Microbiol. 7, 1849–1856 (2022). (PMID: 36192536)
Steele, M. I., Kwong, W. K., Whiteley, M. & Moran, N. A. Diversification of Type VI Secretion System Toxins Reveals Ancient Antagonism among Bee Gut Microbes. MBio 8, e01630–17 (2017). (PMID: 292338935727410)
Koskiniemi, S. et al. Selection of orphan Rhs toxin expression in evolved Salmonella enterica serovar Typhimurium. PLoS Genet 10, e1004255 (2014). (PMID: 246759813967940)
Poole, S. J. et al. Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 7, e1002217 (2011). (PMID: 218293943150448)
Steele, M. I. & Moran, N. A. Evolution of Interbacterial Antagonism in Bee Gut Microbiota Reflects Host and Symbiont Diversification. mSystems 6, e00063–21 (2021). (PMID: 339759638125069)
Petty, N. K., Foulds, I. J., Pradel, E., Ewbank, J. J. & Salmond, G. P. A generalized transducing phage (phiIF3) for the genomically sequenced Serratia marcescens strain Db11: a tool for functional genomics of an opportunistic human pathogen. Microbiology 152, 1701–1708 (2006). (PMID: 16735733)
Gasteiger, E. et al. John M. Walker: Protein identification and analysis tools on the ExPASy server. Proteomics Protoc. Handb. https://doi.org/10.1385/1592598900 .
Kabsch, W. Xds. Acta Crystallogr D. Biol. Crystallogr. 66, 125–132 (2010). (PMID: 201246922815665)
Evans, P. R. An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta. Crystallogr D. Biol. Crystallogr. 67, 282–292 (2011). (PMID: 214604463069743)
Skubak, P. & Pannu, N. S. Automatic protein structure solution from weak X-ray data. Nat. Commun. 4, 2777 (2013). (PMID: 24231803)
Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta. Crystallogr. D. Biol. Crystallogr. 62, 1002–1011 (2006). (PMID: 16929101)
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta. Crystallogr. D. Biol. Crystallogr. 60, 2126–2132 (2004). (PMID: 15572765)
Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta. Crystallogr. D. Biol. Crystallogr. 67, 355–367 (2011). (PMID: 214604543069751)
Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta. Crystallogr. D. Biol. Crystallogr. 66, 12–21 (2010). (PMID: 20057044)
Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545–W549 (2010). (PMID: 204577442896194)
Slabinski, L. et al. XtalPred: a web server for prediction of protein crystallizability. Bioinformatics 23, 3403–3405 (2007). (PMID: 17921170)
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022). (PMID: 356373079184281)
Mariani, V., Biasini, M., Barbato, A. & Schwede, T. lDDT: a local superposition-free score for comparing protein structures and models using distance difference tests. Bioinformatics 29, 2722–2728 (2013). (PMID: 239865683799472)
معلومات مُعتمدة: United Kingdom WT_ Wellcome Trust; 215599/Z/19/Z United Kingdom WT_ Wellcome Trust; 104556/Z/14/Z United Kingdom WT_ Wellcome Trust; 220321/Z/20/Z United Kingdom WT_ Wellcome Trust; MR/N013735/1 United Kingdom MRC_ Medical Research Council
المشرفين على المادة: EC 3.2.2.5 (NAD+ Nucleosidase)
0 (Bacterial Proteins)
0 (Type VI Secretion Systems)
تواريخ الأحداث: Date Created: 20230928 Date Completed: 20231023 Latest Revision: 20231118
رمز التحديث: 20240829
مُعرف محوري في PubMed: PMC10539506
DOI: 10.1038/s41467-023-41751-3
PMID: 37770429
قاعدة البيانات: MEDLINE
الوصف
تدمد:2041-1723
DOI:10.1038/s41467-023-41751-3