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An Intriguing Relationship Between the Cyclic Diguanylate Signaling System and Horizontal Gene Transfer Jonas S An intriguing relationship between the cyclic diguanylate signaling system and horizontal gene transfer Jonas S. Madsen, Ole Hylling, Samuel Jacquiod, Sophie Pécastaings, Lars H. Hansen, Leise Riber, Gisle Vestergaard, Søren J. Sørensen To cite this version: Jonas S. Madsen, Ole Hylling, Samuel Jacquiod, Sophie Pécastaings, Lars H. Hansen, et al.. An intriguing relationship between the cyclic diguanylate signaling system and horizontal gene transfer. ISME Journal, Nature Publishing Group, 2018, 12 (9), pp.2330-2334. 10.1038/s41396-018-0183-0. hal-02135635 HAL Id: hal-02135635 https://hal.archives-ouvertes.fr/hal-02135635 Submitted on 21 May 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. OATAO Open Archive Toulouse Archive Ouverte (OATAO) OATAO is an open access repository that collects the work of some Toulouse researchers and makes it freely available over the web where possible. This is version published in: Official URL: To cite this version: . . . Any correspondence concerning this service should be sent to the repository administrator: [email protected] p-toulouse .fr An intriguing relationsh ip between the cyclic diguanylate signal ing system and horizontal gene transfer Jonas S. Madsen 1 • Oie HyllingG)1'2 • Samuel Jacqu iod(D1 • Sophia Péca staings3 • Lars H. Hansen 2 • Lei se Riber1 • Gisle Vestergaard 1 •S0ren J. S0rensen 1 (1 Abstract The second messenger cyclic diguanylate (c-di-GMP) is ubiquitously used by bacteria to modulate and shift between different pbenotypes including motility, biofilm formation and virulence. Here we show tbat c-di"GMP-associated genes are widespread on plasmids and that enzymes that syntbesize or degrade c-di-GMP are preferentially encoded on transmissible plasmids. Additionally, expression of enzymes that synthesize c-di-GMP was found to increase both biofilm formation and, interestingly, conjugative plasmid traasfer rates. Cyclic di-GMP is a second messenger used by most bacteria proteins [4]. Yet, bacterial genomes typically consist ofboth tbat allows them to control the shift between many pbeno­ chromosomal and extra-chromosomal elements. Plasmids types. The best-studied examples include the transition are extra-chromosomal elements and important facilitators between sessile (biofilm) and planktonic (including motile) of horizontal gene transfer (HOT), which is a main driver of cell states [1] and the expression of virulence factors [2]. bacterial evolution. Horiwntal plasmid transfer typically Higber levels of c-di-GMP aormally promote sessile, low occurs via conjugation. Conjugative plasmids encode a virulent pbeaotypes, whereas lower levels promote plaaktoaic, complete set of transfer genes, while mobilizable plasmids high virulent pbeootypes [3]. c-di -GMP is synthesized by do not and therefore hitchbike on conjugative plasmids. diguanylate cyclases (DGCs) witb GGDEF domains and Conjugative and mobilizable plasmids are collectively degraded by pbospbodiesterases (PDEs) with eitber EAL or called transmissible plasmids [5]. HD-GYP domains [3]. Levels of c-di-GMP are controlled by Here we analyzed available sequences in GenBank and DGCs and PDEs as a response to dues in the environment [3]. made comparative analyses between plasmid- and Many bacteria carry a notably large number of c-di­ chromosome-encoded GGDEF and EAL coding DNA GMP-associated genes on their chromosome: Pseudomonas sequences (CDSs). Our analyses included plasmids that are aeruginosa, for example, encodes 38 GGDEF and/or EAL 10 250 kb long. We used this strict definition to avoid miss­ annotating cloning vectors, chromids, and small chromo­ somes as plasmids. Additionally, metadata available in GenBank was used to determine the replicons as plasmids (https://doi.org/10.1038/s413% 018 0183 0) or chromosomes. We found that both GGDEF and EAL CDSs are corn­ mon on plasmids, as 6.8% of plasmids carried a CDS with a ~ S\àlren J. S\àlren sen GGDEF or EAL domain (Table S1 & S2). Next, GGDEF sjs @bio.ku.dk and EAL CDSs were categorized as catalytically active or inactive based on the presence or absence of conserved 1 Department of Biology, University of Copenbagen, Univers itetsparken 15 , DK 2100 Copenhagen, Denmarlc amino acids in the active sites of the two domains (Fig. S1). Overall, the density of GGDEF and EAL CDSs was higher 2 Department of Environment Sciences, Aarhus University, Frederiksborgvej 399, DK 4(X)() Roskilde, Denmal'k among plasmids compared to chromosomes (Fig. l a). The density of both catalytically active GGDEF and EAL CDSs 3 Laboratoire de Génie Chimique UMR 5503, BioSym Department, Université Paul Sabatier, Université de Toulouse, 35 chemin des was higher on plasmids compared to chromosomes, as was Maraîchers, 31062 Toulouse, France the density of inactive EAL CDSs. The relative density of a b 0 • Klebsiella oxytoga A .0 0 • Klebsiella michiganensis ~ 14 0 • Cronobacter condimenti GGDEF EAL • Klebsiella pneumoniae ST15 gl 12 • Klebsiella pneumoniae U-0608239 • Klebsiella pneumoniae ST48 ~ 10 • • Klebsiella pneumoniae ST23 ü • Escherichia coli C 8 e • Verrucosispora maris ëii O • Sphingopyxis sp. LPB0140 E 6 0 O • Streptomyces avermitilis a "O • • Streptomyces lividans ô 4 • • Streptomyces sp. PVA 94-07 '1:1: 2 O • Streptomyces sp. CCM MD2014 ai O • Streptomyces sp. Tu6071 0 e • Streptomyces sp. FQl ~ • • Streptomyces sp. 14R-10 0 • Streptomyces sp. FR-008 0 • Streptomyces sp. A02 O • Streptomyces bingchenggensis 0 • Streptomyces noursei D Inactive D Active • • Streptomyces sp. FRl • • Streptomyces sp. GBA 94-10 • • Streptomyces sp. FRl • • Streptomyces sp. Tu6071 C • • Streptomyces sp. 769 80 • • Streptomyces davawensis GGDEF EAL • • Streptomyces violaceoruber • • Streptomyces hygroscopicus e • Agrobacterium vitis c 60 O • Neorhizobium galegae e Deinococcus radiodurans o O Deinococcus actinosclerus e • Pantoea vagans O • Rahnella aquatilis • • Rubrobacter radiotolerans 20 0 • Agarivorans gilvus • • Deinococcus proteolyticus O • Alkalilimnicola ehrlichii 0 • • Deinococcus proteolyticus 0 • Deinococcus maricopensis 0 • Pseudomonas putida KT2440 • • Pantoea vagans E 0 Pantoea ananatis O • Aminobacter aminovorans Transmissible Non-transmissible O • Pseudomonas sp. CCOS 191 F D • 99_r-­ L-100-----j • • Ochrobactrum anthropi • • Ochrobactrum anthropi • • Escherichia coli O Anoxybacillus amylolyticus • Alphaproteobacteria • • Synechocystis sp. PCC 6714 O • Desulfarculus baarsii • Gammaproteobacteria 100----c=_ • Legionella pneumophila G • Deltaproteobacteria 0 • Legionella hackeliae • Epsilonproteobacteria • • Campylobacter iguaniorum • Plasmid O • Glaciecola sp. 4H-3-7+YE-5 • Deinococcus-Thermus 0 Chromosome • • Thermovibrio ammonificans • Actinobacteria 0 • Thermovibrio ammonificans •Aquificae • • llyobacter polytropus 0 Bacillus smithii Bacilli 0 • Hydrogenobaculum sp. Y04AAS1 • Cyanobacteria • • Arcobacter butzleri • • Arcobacter butzleri Fig. 1 GGDEFs and EALs are common on transmissible plasmids. a support (1000 replicates) above 90% is shown on branches in gray Density of EAL or GGDEF domain containing CDSs of plasmids and circles. c Percentage of predicted active and inactive GGDEFs and chromosomes. Only replicons with either EAL or GGDEF domains EALs encoded on transmissible or non transmissible plasmids. Ana were included in this analysis. b Maximum likelihood phylogram of lysis made based on plasmids in GenBank with GGDEF or EAL CDSs active only GGDEF proteins identified on plasmids and the most associated with Enterobacteriaceae strains. (A) Enterobacteriaceae similar GGDEFs encoded on chromosomes. Bacterial names refer to cluster; (B) Streptomyces cluster; (C) Rhizobium/Agrobacterium clus the host of the GGDEF CDSs. The phylogram is based on amino acid ter; (D) Deinococcus cluster; (E) Pantoea cluster; (F) Alpha/Gam sequences. Chromosomes were included in the analysis if reported as maproteobacteria cluster; (G) Legionella cluster. complete or chromosome according to NCBI assembly level. Bootstrap inactive GGDEF CDSs was approximately the same GGDEF and EAL domain containing proteins often hold between chromosomes and plasmids. The GGDEF and a diverse array of additional domains important for the EAL domains of plasmids were more diverse (dissimilar) biochemical function of the specific protein. We found a compared to the chromosomal-encoded ones (Fig S2), diverse number of architectures (unique combinations of supporting plasmids as platforms where genetic rearrange- types, number, and sequence of protein domains) of plasmid ment and innovation are more prone to occur. CDSs with active GGDEF and/or EAL domains, illustrating a b e 3.5 0 "00 c:;: 3 ·-u ..Cl::, f2s[j 0 E> 2.5 3 <a':ü 5e c§ -1 o~ Ql o. 0 2 + :.Oc .?! (/) ::::!, - -o.. en __~,g Cl) 1.5 ~~1 E -~ -2 ro o::: Ec Se C ... c::;;::, IDO 1 Ql + (t'.u_ ::, DGC O" '? 0.5 ~ :: -3 Contrai 0 Ec Ko Kp Se SI .2!en C Cil .!= -4 C Ec Se SI d ro Ol i102 ::, Ql C ï:: .2: ~ 8 -5 ? 1§:; 10 È1rr Ql ·- 05 i o:::E en Cil -6 & 0 ë[ Ec Kp Se SI Ec Kp Se SI Fig. 2 Laboratory experiments link the expression
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