Sequential displacement of Type VI Secretion System effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae

Paul C. Kirchberger; Daniel Unterweger; Daniele Provenzano; Stefan Pukatzki; Yan Boucher

doi:10.1038/srep45133

journal article Open Access Mar 22, 2017

Sequential displacement of Type VI Secretion System effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae

Paul C. Kirchberger Daniel Unterweger Daniele Provenzano Stefan Pukatzki Yan Boucher

Scientific Reports Vol. 7 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/srep45133

Abstract

AbstractType VI secretion systems (T6SS) enable bacteria to engage neighboring cells in contact-dependent competition. In Vibrio cholerae, three chromosomal clusters each encode a pair of effector and immunity genes downstream of those encoding the T6SS structural machinery for effector delivery. Different combinations of effector-immunity proteins lead to competition between strains of V. cholerae, which are thought to be protected only from the toxicity of their own effectors. Screening of all publically available V. cholerae genomes showed that numerous strains possess long arrays of orphan immunity genes encoded in the 3′ region of their T6SS clusters. Phylogenetic analysis reveals that these genes are highly similar to those found in the effector-immunity pairs of other strains, indicating acquisition by horizontal gene transfer. Extensive genomic comparisons also suggest that successive addition of effector-immunity gene pairs replaces ancestral effectors, yet retains the cognate immunity genes. The retention of old immunity genes perhaps provides protection against nearby kin bacteria in which the old effector was not replaced. This mechanism, combined with frequent homologous recombination, is likely responsible for the high diversity of T6SS effector-immunity gene profiles observed for V. cholerae and closely related species.

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References

59

[1]

Biodiversity of Vibrios

Fabiano L. Thompson, Tetsuya Iida, Jean Swings

Microbiology and Molecular Biology Reviews 2004 10.1128/mmbr.68.3.403-431.2004

[2]

Kirchberger, P. C. et al. A Small Number of Phylogenetically Distinct Clonal Complexes Dominate a Coastal Vibrio cholerae Population. Applied and environmental microbiology 82, 5576–5586, doi: 10.1128/AEM.01177-16 (2016). 10.1128/aem.01177-16

[3]

Boucher, Y. Sustained Local Diversity of Vibrio cholerae O1 Biotypes in a Previously Cholera-Free Country. mBio 7, e00570–00516, doi: 10.1128/mBio.00570-16 (2016). 10.1128/mbio.00570-16

[4]

Chun, J. et al. Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America 106, 15442–15447, doi: 10.1073/pnas.0907787106 (2009). 10.1073/pnas.0907787106

[5]

Nelson, E. J., Harris, J. B., Morris, J. G. Jr., Calderwood, S. B. & Camilli, A. Cholera transmission: the host, pathogen and bacteriophage dynamic. Nature reviews. Microbiology 7, 693–702, doi: 10.1038/nrmicro2204 (2009). 10.1038/nrmicro2204

[6]

Vezzulli, L., Guzmán, C. A., Colwell, R. R. & Pruzzo, C. Dual role colonization factors connecting Vibrio cholerae’s lifestyles in human and aquatic environments open new perspectives for combating infectious diseases. Current opinion in biotechnology 19, 254–259, doi: 10.1016/j.copbio.2008.04.002 (2008). 10.1016/j.copbio.2008.04.002

[7]

The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer

Sandrine Borgeaud, Lisa C. Metzger, Tiziana Scrignari et al.

Science 2015 10.1126/science.1260064

[8]

Bile Salts Modulate the Mucin-Activated Type VI Secretion System of Pandemic Vibrio cholerae

Verena Bachmann, Benjamin Kostiuk, Daniel Unterweger et al.

PLoS Neglected Tropical Diseases 2015 10.1371/journal.pntd.0004031

[9]

Biogenesis and structure of a type VI secretion membrane core complex

Eric Durand, Van Son Nguyen, Abdelrahim Zoued et al.

Nature 2015 10.1038/nature14667

[10]

Genetic Analysis of Anti-Amoebae and Anti-Bacterial Activities of the Type VI Secretion System in Vibrio cholerae

Jun Zheng, Brian Ho, John J. Mekalanos

PLoS ONE 2011 10.1371/journal.pone.0023876

[11]

Aim, Load, Fire: The Type VI Secretion System, a Bacterial Nanoweapon

Francesca R. Cianfanelli, Laura Monlezun, Sarah J. Coulthurst

Trends in Microbiology 2016 10.1016/j.tim.2015.10.005

[12]

Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin

Stefan Pukatzki, Amy T. Ma, Andrew T. Revel et al.

Proceedings of the National Academy of Sciences 2007 10.1073/pnas.0706532104

[13]

ACD toxin–produced actin oligomers poison formin-controlled actin polymerization

David B. Heisler, Elena Kudryashova, Dmitry O. Grinevich et al.

Science 2015 10.1126/science.aab4090

[14]

Tn-Seq Analysis of Vibrio cholerae Intestinal Colonization Reveals a Role for T6SS-Mediated Antibacterial Activity in the Host

Yang Fu, Matthew K. Waldor, John J. Mekalanos

Cell Host & Microbe 2013 10.1016/j.chom.2013.11.001

[15]

Lytic Activity of the Vibrio cholerae Type VI Secretion Toxin VgrG-3 Is Inhibited by the Antitoxin TsaB

Teresa M. Brooks, Daniel Unterweger, Verena Bachmann et al.

Journal of Biological Chemistry 2013 10.1074/jbc.m112.436725

[16]

VgrG, Tae, Tle, and beyond: the versatile arsenal of Type VI secretion effectors

Eric Durand, Christian Cambillau, Eric Cascales et al.

Trends in Microbiology 2014 10.1016/j.tim.2014.06.004

[17]

The Vibrio cholerae type VI secretion system employs diverse effector modules for intraspecific competition

Daniel Unterweger, Sarah T. Miyata, Verena Bachmann et al.

Nature Communications 2014 10.1038/ncomms4549

[18]

Chimeric adaptor proteins translocate diverse type VI secretion system effectors in Vibrio cholerae

Daniel Unterweger, Benjamin Kostiuk, Rina Ötjengerdes et al.

The EMBO Journal 2015 10.15252/embj.201591163

[19]

Constitutive Type VI Secretion System Expression Gives Vibrio cholerae Intra- and Interspecific Competitive Advantages

Daniel Unterweger, Maya Kitaoka, Sarah T. Miyata et al.

PLoS ONE 2012 10.1371/journal.pone.0048320

[20]

Secretome Analysis of Vibrio cholerae Type VI Secretion System Reveals a New Effector-Immunity Pair

Emrah Altindis, Tao Dong, Christy Catalano et al.

mBio 10.1128/mbio.00075-15

[21]

Labbate, M. et al. A genomic island in Vibrio cholerae with VPI-1 site-specific recombination characteristics contains CRISPR-Cas and type VI secretion modules. Scientific reports 6, doi: 10.1038/srep36891 (2016). 10.1038/srep36891

[22]

Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data

Matthew Kearse, Richard Moir, Amy Wilson et al.

Bioinformatics 2012 10.1093/bioinformatics/bts199

[23]

Gardner, S. N., Slezak, T. & Hall, B. G. kSNP3.0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome. Bioinformatics 31, 2877–2878, doi: 10.1093/bioinformatics/btv271 (2015). 10.1093/bioinformatics/btv271

[24]

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

Alexandros Stamatakis

Bioinformatics 2014 10.1093/bioinformatics/btu033

[25]

Zhaxybayeva, O., Lapierre, P. & Gogarten, J. P. Genome mosaicism and organismal lineages. TRENDS in Genetics 20, 254–260, doi: 10.1016/j.tig.2004.03.009 (2004). 10.1016/j.tig.2004.03.009

[26]

Multiple Sequence Alignment Using ClustalW and ClustalX

Julie D. Thompson, Toby. J. Gibson, Des G. Higgins

Current Protocols in Bioinformatics 10.1002/0471250953.bi0203s00

[27]

Martin, D. P., Murrell, B., Golden, M., Khoosal, A. & Muhire, B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evolution 1, vev003, doi: 10.1093/ve/vev003 (2015). 10.1093/ve/vev003

[28]

Sawyer, S. GENECONV: Statistical tests for detecting gene conversion (version 1.81). Department of Mathematics, Washington University, St. Louis, Mo, doi: 10.1093/oxfordjournals.molbev.a040567 (2000). 10.1093/oxfordjournals.molbev.a040567

[29]

Smith, J. M. Analyzing the mosaic structure of genes. Journal of molecular evolution 34, 126–129, doi: 10.1007/BF00182389 (1992). 10.1007/bf00182389

[30]

Posada, D. & Crandall, K. A. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proceedings of the National Academy of Sciences 98, 13757–13762, doi: 10.1073/pnas.241370698 (2001). 10.1073/pnas.241370698

[31]

Kirchberger, P. C. et al. Vibrio metoecus sp. nov., a close relative of Vibrio cholerae isolated from coastal brackish ponds and clinical specimens. Int J Syst Evol Microbiol 64, 3208–3214, doi: 10.1099/ijs.0.060145-0 (2014). 10.1099/ijs.0.060145-0

[32]

Davis, B. et al. Characterization of biochemically atypical Vibrio cholerae strains and designation of a new pathogenic species, Vibrio mimicus. Journal of clinical microbiology 14, 631–639 (1981). 10.1128/jcm.14.6.631-639.1981

[33]

Zhang, J. et al. Crystallization and preliminary X-ray study of TsiV3 from Vibrio cholerae. Acta Crystallographica Section F: Structural Biology Communications 70, 335–338, doi: 10.1107/S2053230X14001599 (2014). 10.1107/s2053230x14001599

[34]

The type VI secretion system: translocation of effectors and effector-domains

Stefan Pukatzki, Steven B McAuley, Sarah T Miyata

Current Opinion in Microbiology 2009 10.1016/j.mib.2008.11.010

[35]

Dual Expression Profile of Type VI Secretion System Immunity Genes Protects Pandemic Vibrio cholerae

Sarah T. Miyata, Daniel Unterweger, Sydney P. Rudko et al.

PLOS Pathogens 2013 10.1371/journal.ppat.1003752

[36]

A Widespread Bacterial Type VI Secretion Effector Superfamily Identified Using a Heuristic Approach

Alistair B. Russell, Pragya Singh, Mitchell Brittnacher et al.

Cell Host & Microbe 2012 10.1016/j.chom.2012.04.007

[37]

Lysogenic Conversion by a Filamentous Phage Encoding Cholera Toxin

Matthew K. Waldor, John J. Mekalanos

Science 1996 10.1126/science.272.5270.1910

[38]

Karaolis, D. K., Somara, S., Maneval, D. R., Johnson, J. A. & Kaper, J. B. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 399, 375–379, doi: 10.1038/20715 (1999). 10.1038/20715

[39]

Rajanna, C. et al. The vibrio pathogenicity island of epidemic Vibrio cholerae forms precise extrachromosomal circular excision products. Journal of bacteriology 185, 6893–6901, doi: 10.1128/JB.185.23.6893-6901.2003 (2003). 10.1128/jb.185.23.6893-6901.2003

[40]

Riley, M. A. Molecular mechanisms of bacteriocin evolution. Annual review of genetics 32, 255–278, doi: 10.1146/annurev.genet.32.1.255 (1998). 10.1146/annurev.genet.32.1.255

[41]

Prudhomme, M., Libante, V. & Claverys, J. P. Homologous recombination at the border: insertion-deletions and the trapping of foreign DNA in Streptococcus pneumoniae. Proceedings of the National Academy of Sciences of the United States of America 99, 2100–2105, doi: 10.1073/pnas.032262999 (2002). 10.1073/pnas.032262999

[42]

Meier, P. & Wackernagel, W. Mechanisms of homology‐facilitated illegitimate recombination for foreign DNA acquisition in transformable Pseudomonas stutzeri. Molecular microbiology 48, 1107–1118, doi: 10.1046/j.1365-2958.2003.03498.x (2003). 10.1046/j.1365-2958.2003.03498.x

[43]

Selection of Orphan Rhs Toxin Expression in Evolved Salmonella enterica Serovar Typhimurium

Sanna Koskiniemi, Fernando Garza-Sánchez, Linus Sandegren et al.

PLOS Genetics 2014 10.1371/journal.pgen.1004255

[44]

Evolutionary diversification of an ancient gene family (rhs) through C-terminal displacement

Andrew P Jackson, Gavin H Thomas, Julian Parkhill et al.

BMC Genomics 2009 10.1186/1471-2164-10-584

[45]

Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics

Dapeng Zhang, Robson F de Souza, Vivek Anantharaman et al.

Biology Direct 2012 10.1186/1745-6150-7-18

[46]

Identification of Functional Toxin/Immunity Genes Linked to Contact-Dependent Growth Inhibition (CDI) and Rearrangement Hotspot (Rhs) Systems

Stephen J. Poole, Elie J. Diner, Stephanie K. Aoki et al.

PLOS Genetics 2011 10.1371/journal.pgen.1002217

[47]

de Vries, J. & Wackernagel, W. Integration of foreign DNA during natural transformation of Acinetobacter sp. by homology-facilitated illegitimate recombination. Proceedings of the National Academy of Sciences 99, 2094–2099, doi: 10.1073/pnas.042263399 (2002). 10.1073/pnas.042263399

[48]

Orata, F. D. et al. The Dynamics of Genetic Interactions between Vibrio metoecus and Vibrio cholerae, Two Close Relatives Co-Occurring in the Environment. Genome biology and evolution 7, 2941–2954, doi: 10.1093/gbe/evv193 (2015). 10.1093/gbe/evv193

[49]

Keymer, D. P. & Boehm, A. B. Recombination shapes the structure of an environmental Vibrio cholerae population. Applied and environmental microbiology 77, 537–544, doi: 10.1128/AEM.02062-10 (2011). 10.1128/aem.02062-10

[50]

Vos, M. & Didelot, X. A comparison of homologous recombination rates in bacteria and archaea. The ISME journal 3, 199–208, doi: 10.1038/ismej.2008.93 (2009). 10.1038/ismej.2008.93

Showing 50 of 59 references

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Published: Mar 22, 2017
Vol/Issue: 7(1)
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Cite This Article

Paul C. Kirchberger, Daniel Unterweger, Daniele Provenzano, et al. (2017). Sequential displacement of Type VI Secretion System effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae. Scientific Reports, 7(1). https://doi.org/10.1038/srep45133

Sequential displacement of Type VI Secretion System effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae

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