Evolution of the complex transcription network controlling biofilm formation in Candida species

Centro de Investigación y de Estudios Avanzados, Unidad Irapuato, Mexico
Massachusetts Institute of Technology, United States
University College Cork, Ireland
Cell Press, United States
Centers for Disease Control and Prevention, United States
University of Wisconsin, United States
University of California, Merced, United States
Conway Institute, University College Dublin, Ireland
University of California, San Francisco, United States

Apr 7, 2021

Open access
Copyright information

Abstract
Data availability
Article and author information
Metrics

Abstract

We examine how a complex transcription network composed of seven 'master' regulators and hundreds of target genes evolved over a span of approximately 70 million years. The network controls biofilm formation in several Candida species, a group of fungi that are present in humans both as constituents of the microbiota and as opportunistic pathogens. Using a variety of approaches, we observed two major types of changes that have occurred in the biofilm network since the four extant species we examined last shared a common ancestor. Master regulator 'substitutions' occurred over relatively long evolutionary times, resulting in different species having overlapping, but different sets of master regulators of biofilm formation. Second, massive changes in the connections between the master regulators and their target genes occurred over much shorter timescales. We believe this analysis is the first detailed, empirical description of how a complex transcription network has evolved.

Data availability

ChIP-Seq and microarray gene expression data has been deposited to the NCBI Gene Expression Omnibus (GEO) repository under Superseries GSE160783

The following data sets were generated

(2020) Evolution of biofilm formation in Candida
NCBI Gene Expression Omnibus, GSE160783.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE160783

The following previously published data sets were used

1. Holland LM
2. Schröder MS
3. Turner SA
4. Taff H
5. Andes D
6. Grozer Z
7. Gacser A
8. Ames L
9. Haynes K
10. Higgins DG
11. Butler G
(2014) Comparative phenotypic analysis of the major fungal pathogens Candida parapsilosis and Candida albicans
NCBI Gene Expression Omnibus, GSE57451.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE57451
(2012) A Recently Evolved Transcriptional Network Controls Biofilm Development in Candida albicans
NCBI Gene Expression Omnibus, GSE29785.

https://cdn.elifesciences.org/articles/64682/DOI:https://doi.org/10.1016/j.cell.2011.10.048

Article and author information

Author details

Eugenio Mancera

Departamento de Ingeniería Genética, Centro de Investigación y de Estudios Avanzados, Unidad Irapuato, Irapuato, Mexico

For correspondence
eugenio.mancera@cinvestav.mx

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0003-0146-8732
Isabel Nocedal

Department of Biology, Massachusetts Institute of Technology, Cambridge, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-4706-1113
Stephen Hammel

The School of Computer Sciences and IT, University College Cork, Cork, Ireland

Competing interests
No competing interests declared.
Megha Gulati

Molecular Cell, Cell Press, Cambridge, United States

Competing interests
No competing interests declared.
Kaitlin F Mitchell

Center for Global Health, Centers for Disease Control and Prevention, Atlanta, United States

Competing interests
No competing interests declared.
David R Andes

Departments of Medicine and Medical Microbiology and Immunology, University of Wisconsin, Madison, United States

Competing interests
No competing interests declared.
Clarissa J Nobile

Molecular and Cell Biology, University of California, Merced, Merced, United States

Competing interests
Clarissa J Nobile, Clarissa J. Nobile and Alexander D. Johnson are cofounders of BioSynesis, Inc., a company developing diagnostics and therapeutics for biofilm formation..

"This ORCID iD identifies the author of this article:" 0000-0003-0799-6499
Geraldine Butler

School of Biomolecular and Biomedical Science, Conway Institute, University College Dublin, Dublin, Ireland

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-1770-5301
Alexander D Johnson

Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, United States

Competing interests
Alexander D Johnson, Clarissa J. Nobile and Alexander D. Johnson are cofounders of BioSynesis, Inc., a company developing diagnostics and therapeutics for biofilm formation..

Funding

Human Frontiers Science Program (LT000484/2012-L)

Eugenio Mancera

Pew Biomedical Schoolar Award

Clarissa J Nobile

Kamangar family endowed chair

Clarissa J Nobile

UC-MEXUS

Eugenio Mancera

CONACyT (CB-2016-01 282511)

Eugenio Mancera

Wellcome Trust Seed Award in Science (209077/Z/17/Z)

Eugenio Mancera

National Institute of Health (Ro1AI083311)

Alexander D Johnson

National Institute of Health (Ro1AI049187)

Alexander D Johnson

National Institute of Health (Ro1AI073289)

David R Andes

National Institute of Health (R35GM124594)

Clarissa J Nobile

National Institute of Health (R21AI125801)

Clarissa J Nobile

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Procedures were approved by the Institutional Animal Care and Use Committee (IACUC) at the University of Wisconsin, Madison (protocol MV1947).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.