The Candida albicans biofilm gene circuit modulated at the chromatin level by a recent molecular histone innovation.


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
08 2019
Historique:
received: 19 04 2019
accepted: 17 07 2019
revised: 21 08 2019
pubmed: 10 8 2019
medline: 28 2 2020
entrez: 10 8 2019
Statut: epublish

Résumé

Histone H3 and its variants regulate gene expression but the latter are absent in most ascomycetous fungi. Here, we report the identification of a variant histone H3, which we have designated H3VCTG because of its exclusive presence in the CTG clade of ascomycetes, including Candida albicans, a human pathogen. C. albicans grows both as single yeast cells and hyphal filaments in the planktonic mode of growth. It also forms a three-dimensional biofilm structure in the host as well as on human catheter materials under suitable conditions. H3VCTG null (hht1/hht1) cells of C. albicans are viable but produce more robust biofilms than wild-type cells in both in vitro and in vivo conditions. Indeed, a comparative transcriptome analysis of planktonic and biofilm cells reveals that the biofilm circuitry is significantly altered in H3VCTG null cells. H3VCTG binds more efficiently to the promoters of many biofilm-related genes in the planktonic cells than during biofilm growth, whereas the binding of the core canonical histone H3 on the corresponding promoters largely remains unchanged. Furthermore, biofilm defects associated with master regulators, namely, biofilm and cell wall regulator 1 (Bcr1), transposon enhancement control 1 (Tec1), and non-dityrosine 80 (Ndt80), are significantly rescued in cells lacking H3VCTG. The occupancy of the transcription factor Bcr1 at its cognate promoter binding sites was found to be enhanced in the absence of H3VCTG in the planktonic form of growth resulting in enhanced transcription of biofilm-specific genes. Further, we demonstrate that co-occurrence of valine and serine at the 31st and 32nd positions in H3VCTG, respectively, is essential for its function. Taken together, we show that even in a unicellular organism, differential gene expression patterns are modulated by the relative occupancy of the specific histone H3 type at the chromatin level.

Identifiants

pubmed: 31398188
doi: 10.1371/journal.pbio.3000422
pii: PBIOLOGY-D-19-01107
pmc: PMC6703697
doi:

Substances chimiques

Chromatin 0
Fungal Proteins 0
Histones 0
Transcription Factors 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3000422

Subventions

Organisme : NIAID NIH HHS
ID : R01 AI073289
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Science. 1999 Mar 5;283(5407):1535-8
pubmed: 10066176
PLoS Pathog. 2006 Jul;2(7):e63
pubmed: 16839200
Epigenetics Chromatin. 2012 Jun 21;5:7
pubmed: 22650316
Methods Mol Biol. 2016;1356:43-57
pubmed: 26519064
Genetics. 2002 Mar;160(3):961-73
pubmed: 11901114
FEBS J. 2005 Oct;272(20):5149-68
pubmed: 16218948
Cell. 2012 Jan 20;148(1-2):126-38
pubmed: 22265407
BMC Genomics. 2013 Apr 02;14:212
pubmed: 23547856
Mol Cell Biol. 2006 Oct;26(20):7719-30
pubmed: 16908532
J Microbiol. 2011 Apr;49(2):171-7
pubmed: 21538235
Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6428-35
pubmed: 16571659
Med Mycol. 2008 Feb;46(1):1-15
pubmed: 17852717
Mol Cells. 2012 Feb;33(2):183-93
pubmed: 22358510
PLoS One. 2009 Nov 24;4(11):e7967
pubmed: 19956771
PLoS One. 2013 Dec 05;8(12):e82395
pubmed: 24349274
Microbiol Mol Biol Rev. 2008 Sep;72(3):495-544
pubmed: 18772287
Sci Adv. 2015;1(3):e1500248
pubmed: 25977940
Science. 1997 Jul 4;277(5322):105-9
pubmed: 9204892
Exp Gerontol. 1999 Sep;34(6):741-54
pubmed: 10579635
PLoS Pathog. 2012;8(4):e1002585
pubmed: 22496639
Biochimie. 2005 Sep-Oct;87(9-10):827-34
pubmed: 16164992
PLoS Genet. 2009 Dec;5(12):e1000783
pubmed: 20041210
Curr Opin Genet Dev. 2010 Apr;20(2):110-7
pubmed: 20153629
Virulence. 2013 Feb 15;4(2):119-28
pubmed: 23302789
Nat Protoc. 2008;3(6):1101-8
pubmed: 18546601
Cell. 1997 Sep 5;90(5):939-49
pubmed: 9298905
Science. 1994 Dec 9;266(5191):1723-6
pubmed: 7992058
Science. 1985 Nov 8;230(4726):666-9
pubmed: 3901258
J Med Microbiol. 1999 Jul;48(7):671-679
pubmed: 10403418
Genome Res. 2002 Dec;12(12):1921-8
pubmed: 12466296
Dev Cell. 2010 Nov 16;19(5):662-74
pubmed: 21074717
Development. 2013 Jun;140(12):2513-24
pubmed: 23715545
Curr Opin Struct Biol. 2013 Feb;23(1):109-15
pubmed: 23265997
Mol Microbiol. 2015 Jun;96(6):1226-39
pubmed: 25784162
PLoS Genet. 2016 Feb 04;12(2):e1005839
pubmed: 26845548
J Med Microbiol. 1998 Mar;47(3):253-6
pubmed: 9511830
Cell Microbiol. 2002 Mar;4(3):127-37
pubmed: 11906450
mSphere. 2016 Jun 15;1(3):
pubmed: 27340698
Microbiol Spectr. 2015 Jun;3(3):
pubmed: 26185083
mBio. 2016 Sep 13;7(5):
pubmed: 27624133
Curr Biol. 2005 Jun 21;15(12):1150-5
pubmed: 15964282
Mol Biol Cell. 2015 Mar 15;26(6):1174-87
pubmed: 25609092
Mol Biol Cell. 2007 Mar;18(3):815-26
pubmed: 17182857
Cell Res. 2011 Mar;21(3):421-34
pubmed: 21263457
Infect Immun. 2004 Oct;72(10):6023-31
pubmed: 15385506
Nat Rev Genet. 2014 Apr;15(4):259-71
pubmed: 24614311
Elife. 2016 Sep 10;5:
pubmed: 27614020
Eukaryot Cell. 2003 Dec;2(6):1266-73
pubmed: 14665461
Int J Dev Biol. 2009;53(2-3):231-43
pubmed: 19412883
Annu Rev Microbiol. 2015;69:71-92
pubmed: 26488273
Nat Protoc. 2008;3(4):698-709
pubmed: 18388953
Expert Rev Anti Infect Ther. 2012 Jan;10(1):85-93
pubmed: 22149617
Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12969-74
pubmed: 12271118
Trends Genet. 2013 Nov;29(11):630-40
pubmed: 23830582
Mol Cell. 2002 Jun;9(6):1191-200
pubmed: 12086617
Nat Commun. 2018 Jun 8;9(1):2253
pubmed: 29884848
Clin Microbiol Rev. 2002 Apr;15(2):167-93
pubmed: 11932229
Genomics. 2002 Nov;80(5):487-98
pubmed: 12408966
Gene. 2004 Oct 27;341:119-27
pubmed: 15474295

Auteurs

Laxmi Shanker Rai (LS)

Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India.
Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, USC2019 INRA, Paris, France.

Rima Singha (R)

Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India.

Hiram Sanchez (H)

Department of Medicine, University of Wisconsin, Madison, Wisconsin, United States of America.

Tanmoy Chakraborty (T)

Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India.

Bipin Chand (B)

Genotypic Technology Private Limited, Bangalore, India.

Sophie Bachellier-Bassi (S)

Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, USC2019 INRA, Paris, France.

Shantanu Chowdhury (S)

GNR Center for Genome Informatics, CSIR-Institute of Genomics and Integrative Biology, New Delhi, India.
Proteomics and Structural Biology Unit, CSIR-Institute of Genomics and Integrative Biology, New Delhi, India.

Christophe d'Enfert (C)

Unité Biologie et Pathogénicité Fongiques, Institut Pasteur, USC2019 INRA, Paris, France.

David R Andes (DR)

Department of Medicine, University of Wisconsin, Madison, Wisconsin, United States of America.

Kaustuv Sanyal (K)

Molecular Mycology Laboratory, Molecular Biology and Genetics Unit, Jawaharlal Nehru Centre for Advanced Scientific Research, Bangalore, India.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH