The small-secreted cysteine-rich protein CyrA is a virulence factor participating in the attack of Caenorhabditis elegans by Duddingtonia flagrans.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
11 2021
Historique:
received: 24 06 2021
accepted: 11 10 2021
entrez: 4 11 2021
pubmed: 5 11 2021
medline: 15 12 2021
Statut: epublish

Résumé

Nematode-trapping fungi (NTF) are a diverse and intriguing group of fungi that live saprotrophically but can switch to a predatory lifestyle when starving and in the presence of nematodes. NTF like Arthrobotrys oligospora or Duddingtonia flagrans produce adhesive trapping networks to catch and immobilize nematodes. After penetration of the cuticle, hyphae grow and develop inside the worm and secrete large amounts of hydrolytic enzymes for digestion. In many microbial pathogenic interactions small-secreted proteins (SSPs) are used to manipulate the host. The genome of D. flagrans encodes more than 100 of such putative SSPs one of which is the cysteine-rich protein CyrA. We have chosen this gene for further analysis because it is only found in NTF and appeared to be upregulated during the interaction. We show that the cyrA gene was transcriptionally induced in trap cells, and the protein accumulated at the inner rim of the hyphal ring before Caenorhabditis elegans capture. After worm penetration, the protein appeared at the fungal infection bulb, where it is likely to be secreted with the help of the exocyst complex. A cyrA-deletion strain was less virulent, and the time from worm capture to paralysis was extended. Heterologous expression of CyrA in C. elegans reduced its lifespan. CyrA accumulated in C. elegans in coelomocytes where the protein possibly is inactivated. This is the first example that SSPs may be important in predatory microbial interactions.

Identifiants

pubmed: 34735554
doi: 10.1371/journal.ppat.1010028
pii: PPATHOGENS-D-21-01312
pmc: PMC8568293
doi:

Substances chimiques

CCN Intercellular Signaling Proteins 0
Fungal Proteins 0
Cysteine K848JZ4886

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1010028

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Nucleic Acids Res. 2006 Jan 1;34(Database issue):D459-64
pubmed: 16381911
PLoS One. 2015 Jul 15;10(7):e0133085
pubmed: 26177455
Gene. 1996 Apr 17;170(1):131-5
pubmed: 8621073
Genetics. 2001 Sep;159(1):133-45
pubmed: 11560892
J Vis Exp. 2012 Jun 10;(64):e4019
pubmed: 22710399
Zoology (Jena). 2016 Aug;119(4):350-8
pubmed: 27448694
BMC Vet Res. 2009 Dec 28;5:46
pubmed: 20038297
Proc Natl Acad Sci U S A. 2010 Apr 20;107(16):7359-64
pubmed: 20368449
Endocrinology. 2001 Feb;142(2):864-73
pubmed: 11159860
mBio. 2021 Mar 30;12(2):
pubmed: 33785621
Nat Commun. 2013;4:1996
pubmed: 23774898
Development. 2015 Dec 15;142(24):4374-84
pubmed: 26552885
Proc Natl Acad Sci U S A. 2007 May 15;104(20):8379-84
pubmed: 17494736
J Fungi (Basel). 2020 Oct 04;6(4):
pubmed: 33020457
Appl Environ Microbiol. 2006 Jul;72(7):5020-6
pubmed: 16820501
Adv Exp Med Biol. 2010;708:105-21
pubmed: 21528695
Annu Rev Phytopathol. 2019 Aug 25;57:411-430
pubmed: 31337276
Plant Cell. 2010 Apr;22(4):1388-403
pubmed: 20435900
Nature. 2020 Aug;584(7821):410-414
pubmed: 32641833
BMC Biol. 2016 Apr 29;14:35
pubmed: 27129311
Adv Exp Med Biol. 2012;710:29-36
pubmed: 22127883
New Phytol. 2020 Jul;227(2):326-333
pubmed: 32239533
Nat Rev Microbiol. 2017 Jul;15(7):409-421
pubmed: 28479603
mSphere. 2017 Nov 22;2(6):
pubmed: 29202039
Vet Clin North Am Food Anim Pract. 2020 Mar;36(1):89-107
pubmed: 32029191
Antonie Van Leeuwenhoek. 1985;51(4):399-407
pubmed: 4091542
Nat Commun. 2020 Nov 17;11(1):5845
pubmed: 33203871
J Cell Biol. 1995 Jul;130(2):299-312
pubmed: 7615633
BMC Genomics. 2014 Nov 11;15:968
pubmed: 25384908
Curr Biol. 2013 Jan 7;23(1):83-6
pubmed: 23246407
Elife. 2017 Jan 18;6:
pubmed: 28098555
J Nematol. 1980 Oct;12(4):244-52
pubmed: 19300699
Exp Parasitol. 2017 Apr;175:74-78
pubmed: 28192084
Nat Struct Mol Biol. 2005 Dec;12(12):1094-100
pubmed: 16249794
Mol Plant Pathol. 2018 Sep;19(9):2094-2110
pubmed: 29569316
Int J Health Serv. 1991;21(4):731-57
pubmed: 1769760
PLoS Pathog. 2016 Oct 6;12(10):e1005921
pubmed: 27711180
EFSA J. 2020 Jul 23;18(7):e06208
pubmed: 32714465
Phytopathology. 2021 Mar;111(3):474-477
pubmed: 33021880
Curr Biol. 2011 Jul 26;21(14):1204-9
pubmed: 21757354
Curr Opin Plant Biol. 2015 Dec;28:48-54
pubmed: 26453967
Microbiologyopen. 2015 Dec;4(6):952-66
pubmed: 26472068
Nat Commun. 2021 Sep 15;12(1):5462
pubmed: 34526503
Antonie Van Leeuwenhoek. 2021 Jul;114(7):885-912
pubmed: 33893903
Appl Environ Microbiol. 2013 Aug;79(16):4993-5004
pubmed: 23770896
Plant Cell. 2015 Nov;27(11):3277-89
pubmed: 26566920
J Mol Neurosci. 2004;22(1-2):63-71
pubmed: 14742911
Microbiol Spectr. 2017 Jan;5(1):
pubmed: 28128072
Annu Rev Plant Biol. 2015;66:513-45
pubmed: 25923844
Antonie Van Leeuwenhoek. 1985;51(4):385-98
pubmed: 4091541
Plant Cell. 2002 Sep;14(9):2107-19
pubmed: 12215509
PLoS Pathog. 2014 Jul 03;10(7):e1003866
pubmed: 24992561
Environ Microbiol. 2008 Feb;10(2):364-75
pubmed: 18028414
Cell. 1999 Apr 16;97(2):153-5
pubmed: 10219235
Annu Rev Phytopathol. 1998;36:165-205
pubmed: 15012497
Exp Parasitol. 2015 Dec;159:1-4
pubmed: 26208781
Plant Signal Behav. 2019;14(2):1557008
pubmed: 30621489
J Cell Sci. 2007 Sep 1;120(Pt 17):3099-110
pubmed: 17698923
FASEB J. 2010 Feb;24(2):383-92
pubmed: 19783783
Adv Microb Physiol. 1994;36:111-43
pubmed: 7942313
Nat Commun. 2014 Aug 26;5:4686
pubmed: 25156390
Front Plant Sci. 2021 Jun 04;12:687713
pubmed: 34149788
Nat Commun. 2018 Dec 3;9(1):5140
pubmed: 30510181
Proc Natl Acad Sci U S A. 2012 Jul 3;109(27):10960-5
pubmed: 22715289
Mol Endocrinol. 2008 Dec;22(12):2583-95
pubmed: 18669645
Nat Cell Biol. 1999 May;1(1):E17-22
pubmed: 10559876
Curr Biol. 2013 Oct 7;23(19):R862-4
pubmed: 24112976
Vet Clin North Am Food Anim Pract. 2018 Mar;34(1):185-199
pubmed: 29421029
PLoS Genet. 2019 Mar 27;15(3):e1008029
pubmed: 30917129
Antonie Van Leeuwenhoek. 1989 Oct;56(3):251-61
pubmed: 2589853

Auteurs

Nicole Wernet (N)

Karlsruhe Institute of Technology (KIT)-South Campus, Institute for Applied Biosciences, Dept. of Microbiology, Karlsruhe, Germany.

Valentin Wernet (V)

Karlsruhe Institute of Technology (KIT)-South Campus, Institute for Applied Biosciences, Dept. of Microbiology, Karlsruhe, Germany.

Reinhard Fischer (R)

Karlsruhe Institute of Technology (KIT)-South Campus, Institute for Applied Biosciences, Dept. of Microbiology, Karlsruhe, Germany.

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Classifications MeSH