Transcription activator-like effector protects bacterial endosymbionts from entrapment within fungal hyphae.

Mucoromycota Mycetohabitans compartmentalization intracellular survival microfluidics symbiosis

Journal

Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782

Informations de publication

Date de publication:
10 07 2023
Historique:
received: 04 11 2022
revised: 30 03 2023
accepted: 12 05 2023
medline: 13 7 2023
pubmed: 11 6 2023
entrez: 10 6 2023
Statut: ppublish

Résumé

As an endosymbiont of the ecologically and medically relevant fungus Rhizopus microsporus, the toxin-producing bacterium Mycetohabitans rhizoxinica faces myriad challenges, such as evading the host's defense mechanisms. However, the bacterial effector(s) that facilitate the remarkable ability of M. rhizoxinica to freely migrate within fungal hyphae have thus far remained unknown. Here, we show that a transcription activator-like (TAL) effector released by endobacteria is an essential symbiosis factor. By combining microfluidics with fluorescence microscopy, we observed enrichment of TAL-deficient M. rhizoxinica in side hyphae. High-resolution live imaging showed the formation of septa at the base of infected hyphae, leading to the entrapment of endobacteria. Using a LIVE/DEAD stain, we demonstrate that the intracellular survival of trapped TAL-deficient bacteria is significantly reduced compared with wild-type M. rhizoxinica, indicative of a protective host response in the absence of TAL proteins. Subversion of host defense in TAL-competent endobacteria represents an unprecedented function of TAL effectors. Our data illustrate an unusual survival strategy of endosymbionts in the host and provide deeper insights into the dynamic interactions between bacteria and eukaryotes.

Identifiants

pubmed: 37301202
pii: S0960-9822(23)00623-1
doi: 10.1016/j.cub.2023.05.028
pmc: PMC10337650
pii:
doi:

Substances chimiques

Transcription Activator-Like Effectors 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2646-2656.e4

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

New Phytol. 2012 Dec;196(4):1197-1207
pubmed: 23078195
Genes (Basel). 2018 Aug 01;9(8):
pubmed: 30071618
J Am Chem Soc. 2006 Sep 6;128(35):11529-36
pubmed: 16939276
Curr Biol. 2007 May 1;17(9):773-7
pubmed: 17412585
Science. 2007 Oct 26;318(5850):645-8
pubmed: 17962564
Proc Natl Acad Sci U S A. 2016 Dec 27;113(52):15102-15107
pubmed: 27956601
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Fungal Genet Biol. 2002 Oct;37(1):109-19
pubmed: 12223195
Curr Opin Microbiol. 2009 Feb;12(1):37-43
pubmed: 19168386
Environ Sci Technol. 2005 Jun 15;39(12):4640-6
pubmed: 16047804
Annu Rev Phytopathol. 2019 Aug 25;57:459-481
pubmed: 31387457
Sci Rep. 2014 Jan 23;4:3831
pubmed: 24452192
PNAS Nexus. 2022 Aug 08;1(4):pgac152
pubmed: 36714835
Sci Rep. 2019 Apr 24;9(1):6483
pubmed: 31019274
Curr Opin Microbiol. 2011 Feb;14(1):47-53
pubmed: 21215685
Org Biomol Chem. 2018 Sep 26;16(37):8345-8352
pubmed: 30209475
Angew Chem Int Ed Engl. 2010 Oct 4;49(41):7476-80
pubmed: 20718018
FEMS Microbiol Ecol. 2017 Jan;93(1):
pubmed: 27797964
New Phytol. 2013 Aug;199(3):773-86
pubmed: 23692030
Science. 2009 Dec 11;326(5959):1509-12
pubmed: 19933107
BMC Microbiol. 2015 Feb 18;15:36
pubmed: 25881030
Nucleic Acids Res. 2014 Jun;42(11):7436-49
pubmed: 24792163
Annu Rev Phytopathol. 2018 Aug 25;56:289-309
pubmed: 30149793
Angew Chem Int Ed Engl. 2012 Sep 17;51(38):9615-8
pubmed: 22915379
Curr Top Microbiol Immunol. 2013;358:215-43
pubmed: 22076025
Curr Biol. 2012 Jul 24;22(14):R555-61
pubmed: 22835786
Proc Natl Acad Sci U S A. 2020 Jul 21;117(29):17122-17129
pubmed: 32632014
Curr Biol. 2019 Jan 21;29(2):217-228.e4
pubmed: 30612903
ISME J. 2011 Feb;5(2):252-61
pubmed: 20720578
Acta Crystallogr F Struct Biol Commun. 2014 Jan;70(Pt 1):87-91
pubmed: 24419625
Appl Environ Microbiol. 2009 May;75(9):2982-6
pubmed: 19286793
Fungal Genet Biol. 1998 Feb;23(1):45-56
pubmed: 9514694
Elife. 2019 Sep 17;8:
pubmed: 31526474
J Bacteriol. 2011 Feb;193(3):783-4
pubmed: 21131495
Nature. 2005 Oct 6;437(7060):884-8
pubmed: 16208371
Proc Natl Acad Sci U S A. 2011 Jun 28;108 Suppl 2:10800-7
pubmed: 21690339
ISME J. 2008 Jun;2(6):632-41
pubmed: 18309361
Elife. 2014 Sep 02;3:e03007
pubmed: 25182414
mBio. 2020 Sep 8;11(5):
pubmed: 32900811
PLoS Pathog. 2011 Jun;7(6):e1002096
pubmed: 21738468
ISME J. 2014 Feb;8(2):257-70
pubmed: 24008325
Philos Trans R Soc Lond B Biol Sci. 2020 Sep 28;375(1808):20190602
pubmed: 32772665
Integr Biol (Camb). 2014 Oct;6(10):935-45
pubmed: 25144657
Mol Plant Pathol. 2014 Aug;15(6):531-4
pubmed: 25041428
Fungal Genet Biol. 2007 Nov;44(11):1077-84
pubmed: 17434770
Chembiochem. 2015 Feb 9;16(3):387-92
pubmed: 25530287
Chembiochem. 2007 Jan 2;8(1):41-5
pubmed: 17154220
Cell Microbiol. 2012 May;14(5):622-33
pubmed: 22289128
ISME J. 2017 Aug;11(8):1727-1735
pubmed: 28387771

Auteurs

Ingrid Richter (I)

Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology, HKI, Beutenbergstr. 11a, 07745 Jena, Germany.

Philipp Wein (P)

Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology, HKI, Beutenbergstr. 11a, 07745 Jena, Germany.

Zerrin Uzum (Z)

Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology, HKI, Beutenbergstr. 11a, 07745 Jena, Germany.

Claire E Stanley (CE)

Department of Bioengineering, Imperial College, South Kensington, London SW7 2AZ, UK.

Jana Krabbe (J)

Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology, HKI, Beutenbergstr. 11a, 07745 Jena, Germany.

Evelyn M Molloy (EM)

Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology, HKI, Beutenbergstr. 11a, 07745 Jena, Germany.

Nadine Moebius (N)

Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology, HKI, Beutenbergstr. 11a, 07745 Jena, Germany.

Iuliia Ferling (I)

Junior Research Group Evolution of Microbial Interactions, Leibniz Institute for Natural Product Research and Infection Biology, Beutenbergstr. 11a, 07745 Jena, Germany.

Falk Hillmann (F)

Junior Research Group Evolution of Microbial Interactions, Leibniz Institute for Natural Product Research and Infection Biology, Beutenbergstr. 11a, 07745 Jena, Germany.

Christian Hertweck (C)

Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology, HKI, Beutenbergstr. 11a, 07745 Jena, Germany; Institute of Microbiology, Faculty of Biological Sciences, Friedrich Schiller University Jena, 07743 Jena, Germany. Electronic address: christian.hertweck@leibniz-hki.de.

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