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Title: Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins

Abstract

Tailocins are bactericidal protein complexes produced by a wide variety of bacteria that kill closely related strains and may play a role in microbial community structure. Thanks to their high specificity, tailocins have been proposed as precision antibacterial agents for therapeutic applications. Compared to tailed phages, with whom they share an evolutionary and morphological relationship, bacterially produced tailocins kill their host upon production but producing strains display resistance to self-intoxication. Though lipopolysaccharide (LPS) has been shown to act as a receptor for tailocins, the breadth of factors involved in tailocin sensitivity, and the mechanisms behind resistance to self-intoxication, remain unclear. Here, we employed genome-wide screens in four non-model pseudomonads to identify mutants with altered fitness in the presence of tailocins produced by closely related pseudomonads. Our mutant screens identified O-antigen composition and display as most important in defining sensitivity to our tailocins. In addition, the screens suggest LPS thinning as a mechanism by which resistant strains can become more sensitive to tailocins. We validate many of these novel findings, and extend these observations of tailocin sensitivity to 130 genome-sequenced pseudomonads. This work offers insights into tailocin-bacteria interactions, informing the potential use of tailocins in microbiome manipulation and antibacterial therapy.

Authors:
 [1];  [2];  [3];  [3];  [3];  [3];  [3]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [4]
  1. Univ. of California, Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States). Innovative Genomics Inst.
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Univ. of California, Berkeley, CA (United States). Innovative Genomics Inst.; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Science Foundation (NSF); National Center for Advancing Translational Sciences
OSTI Identifier:
1773739
Alternate Identifier(s):
OSTI ID: 1777972
Grant/Contract Number:  
AC02-05CH11231; S10RR025622; S10RR029668; S10RR027303; OD018174; DGE 1752814
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 15; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Bacterial genetics; functional genomics; microbial ecology; soil microbiology

Citation Formats

Carim, Sean, Azadeh, Ashley L., Kazakov, Alexey E., Price, Morgan N., Walian, Peter J., Lui, Lauren M., Nielsen, Torben N., Chakraborty, Romy, Deutschbauer, Adam M., Mutalik, Vivek K., and Arkin, Adam P. Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins. United States: N. p., 2021. Web. doi:10.1038/s41396-021-00921-1.
Carim, Sean, Azadeh, Ashley L., Kazakov, Alexey E., Price, Morgan N., Walian, Peter J., Lui, Lauren M., Nielsen, Torben N., Chakraborty, Romy, Deutschbauer, Adam M., Mutalik, Vivek K., & Arkin, Adam P. Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins. United States. https://doi.org/10.1038/s41396-021-00921-1
Carim, Sean, Azadeh, Ashley L., Kazakov, Alexey E., Price, Morgan N., Walian, Peter J., Lui, Lauren M., Nielsen, Torben N., Chakraborty, Romy, Deutschbauer, Adam M., Mutalik, Vivek K., and Arkin, Adam P. Mon . "Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins". United States. https://doi.org/10.1038/s41396-021-00921-1. https://www.osti.gov/servlets/purl/1773739.
@article{osti_1773739,
title = {Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins},
author = {Carim, Sean and Azadeh, Ashley L. and Kazakov, Alexey E. and Price, Morgan N. and Walian, Peter J. and Lui, Lauren M. and Nielsen, Torben N. and Chakraborty, Romy and Deutschbauer, Adam M. and Mutalik, Vivek K. and Arkin, Adam P.},
abstractNote = {Tailocins are bactericidal protein complexes produced by a wide variety of bacteria that kill closely related strains and may play a role in microbial community structure. Thanks to their high specificity, tailocins have been proposed as precision antibacterial agents for therapeutic applications. Compared to tailed phages, with whom they share an evolutionary and morphological relationship, bacterially produced tailocins kill their host upon production but producing strains display resistance to self-intoxication. Though lipopolysaccharide (LPS) has been shown to act as a receptor for tailocins, the breadth of factors involved in tailocin sensitivity, and the mechanisms behind resistance to self-intoxication, remain unclear. Here, we employed genome-wide screens in four non-model pseudomonads to identify mutants with altered fitness in the presence of tailocins produced by closely related pseudomonads. Our mutant screens identified O-antigen composition and display as most important in defining sensitivity to our tailocins. In addition, the screens suggest LPS thinning as a mechanism by which resistant strains can become more sensitive to tailocins. We validate many of these novel findings, and extend these observations of tailocin sensitivity to 130 genome-sequenced pseudomonads. This work offers insights into tailocin-bacteria interactions, informing the potential use of tailocins in microbiome manipulation and antibacterial therapy.},
doi = {10.1038/s41396-021-00921-1},
journal = {The ISME Journal},
number = ,
volume = 15,
place = {United States},
year = {Mon Mar 01 00:00:00 EST 2021},
month = {Mon Mar 01 00:00:00 EST 2021}
}

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  • DOI: 10.1071/sb15001

Chromosome-level genome assembly of Aldrichina grahami, a forensically important blowfly
journal, March 2020


Hymenoscyphus pusillus , a new species on leaves of Fraxinus pennsylvanica in Poland
journal, December 2018


Did aculeate silk evolve as an antifouling material?
journal, September 2018


Computational approaches to study the effects of small genomic variations
journal, September 2015

  • Khafizov, Kamil; Ivanov, Maxim V.; Glazova, Olga V.
  • Journal of Molecular Modeling, Vol. 21, Issue 10
  • DOI: 10.1007/s00894-015-2794-y

The complete mitochondrial genome of the Xinyuan honey bee, Apis mellifera sinisxinyuan (Insecta: Hymenoptera: Apidae)
journal, January 2020


Characterization of the lytic archaeal virus Drs3 infecting Methanobacterium formicicum
journal, December 2018


Evolution and development of the adelphophagic, intracapsular Schmidt’s larva of the nemertean Lineus ruber
journal, September 2015


Glutathione S-Transferase (GST) Gene Diversity in the Crustacean Calanus finmarchicus – Contributors to Cellular Detoxification
journal, May 2015


The genetic architecture of low-temperature adaptation in the wine yeast Saccharomyces cerevisiae
journal, February 2017


Agriculturally dominated landscapes reduce bee phylogenetic diversity and pollination services
journal, January 2019


Computational studies of human class V alcohol dehydrogenase - the odd sibling
journal, July 2016


Duplication and Remolding of tRNA Genes in the Mitochondrial Genome of Reduvius tenebrosus (Hemiptera: Reduviidae)
journal, June 2016

  • Jiang, Pei; Li, Hu; Song, Fan
  • International Journal of Molecular Sciences, Vol. 17, Issue 6
  • DOI: 10.3390/ijms17060951

Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina
journal, February 2019

  • Morin, Emmanuelle; Miyauchi, Shingo; San Clemente, Hélène
  • New Phytologist, Vol. 222, Issue 3
  • DOI: 10.1111/nph.15687

Plastid Genome Evolution in the Early-Diverging Legume Subfamily Cercidoideae (Fabaceae)
journal, February 2018


Genome Sequences of Akhmeta Virus, an Early Divergent Old World Orthopoxvirus
journal, May 2018

  • Gao, Jinxin; Gigante, Crystal; Khmaladze, Ekaterine
  • Viruses, Vol. 10, Issue 5
  • DOI: 10.3390/v10050252

Poliovirus serotype 2 and coxsackievirus A promote the natural recombination of poliovirus
journal, November 2019

  • Qian, Yongjiang; Pu, Xufeng; Yu, Yu
  • Journal of Medical Virology, Vol. 92, Issue 3
  • DOI: 10.1002/jmv.25620

Reconstructing the genetic history of late Neanderthals
journal, March 2018

  • Hajdinjak, Mateja; Fu, Qiaomei; Hübner, Alexander
  • Nature, Vol. 555, Issue 7698
  • DOI: 10.1038/nature26151

Climate and host‐plant associations shaped the evolution of ceutorhynch weevils throughout the Cenozoic
journal, August 2018

  • Letsch, Harald; Gottsberger, Brigitte; Metzl, Christian
  • Evolution, Vol. 72, Issue 9
  • DOI: 10.1111/evo.13520

Detection of H3N8 influenza A virus with multiple mammalian-adaptive mutations in a rescued Grey seal (Halichoerus grypus) pup
journal, January 2020

  • Venkatesh, Divya; Bianco, Carlo; Núñez, Alejandro
  • Virus Evolution, Vol. 6, Issue 1
  • DOI: 10.1093/ve/veaa016

Diversity and Hidden Host Specificity of Chytrids Infecting Colonial Volvocacean Algae
journal, June 2018

  • Van den Wyngaert, Silke; Rojas-Jimenez, Keilor; Seto, Kensuke
  • Journal of Eukaryotic Microbiology, Vol. 65, Issue 6
  • DOI: 10.1111/jeu.12632

Biodiversity of Magnetotactic Bacteria in the Freshwater Lake Beloe Bordukovskoe, Russia
journal, May 2020


Interlaboratory Comparison of Six Real-Time PCR Assays for Detection of Bovine Leukemia Virus Proviral DNA
journal, July 2018

  • Jaworski, J. P.; Pluta, A.; Rola-Łuszczak, M.
  • Journal of Clinical Microbiology, Vol. 56, Issue 7
  • DOI: 10.1128/JCM.00304-18

The complete chloroplast genome of Rosa berberifolia
journal, January 2019


Diversification patterns in the CES clade (Brassicaceae tribes Cremolobeae, Eudemeae, Schizopetaleae) in Andean South America
journal, May 2016

  • Salariato, Diego L.; Zuloaga, Fernando O.; Franzke, Andreas
  • Botanical Journal of the Linnean Society, Vol. 181, Issue 4
  • DOI: 10.1111/boj.12430

OD-seq: outlier detection in multiple sequence alignments
journal, August 2015


Molecular Diversification of the Seminal Fluid Proteome in a Recently Diverged Passerine Species Pair
journal, October 2019

  • Rowe, Melissah; Whittington, Emma; Borziak, Kirill
  • Molecular Biology and Evolution, Vol. 37, Issue 2
  • DOI: 10.1093/molbev/msz235

A continuous morphological approach to study the evolution of pollen in a phylogenetic context: An example with the order Myrtales
text, January 2017

  • Kriebel, Ricardo; Khabbazian, Mohammad Hassan; Sytsma, Kenneth J.
  • Columbia University
  • DOI: 10.7916/d85m7nnt

Complete chloroplast genome of Exacum affine (Gentianaceae): the first plastome of the tribe Exaceae in the family Gentianaceae
journal, July 2019


Prevotella intermedia produces two proteins homologous to Porphyromonas gingivalis HmuY but with different heme coordination mode
journal, January 2020

  • Bielecki, Marcin; Antonyuk, Svetlana; Strange, Richard W.
  • Biochemical Journal, Vol. 477, Issue 2
  • DOI: 10.1042/bcj20190607

The complete chloroplast genome and phylogenetic analysis of Begonia pulchrifolia , a near endangered Begoniaceae plant
journal, July 2019


Piggy: a rapid, large-scale pan-genome analysis tool for intergenic regions in bacteria
journal, March 2018


Spatial transmission of H5N6 highly pathogenic avian influenza viruses among wild birds in Ibaraki Prefecture, Japan, 2016–2017
journal, February 2018