Genetic and behavioral adaptation of Candida parapsilosis to the microbiome of hospitalized infants revealed by in situ genomics, transcriptomics, and proteomics
Abstract
Background Candida parapsilosis is a common cause of invasive candidiasis, especially in newborn infants, and infections have been increasing over the past two decades. C. parapsilosis has been primarily studied in pure culture, leaving gaps in understanding of its function in a microbiome context. Results. Here, we compare five unique C. parapsilosis genomes assembled from premature infant fecal samples, three of which are newly reconstructed, and analyze their genome structure, population diversity, and in situ activity relative to reference strains in pure culture. All five genomes contain hotspots of single nucleotide variants, some of which are shared by strains from multiple hospitals. A subset of environmental and hospital-derived genomes share variants within these hotspots suggesting derivation of that region from a common ancestor. Four of the newly reconstructed C. parapsilosis genomes have 4 to 16 copies of the gene RTA3, which encodes a lipid translocase and is implicated in antifungal resistance, potentially indicating adaptation to hospital antifungal use. Time course metatranscriptomics and metaproteomics on fecal samples from a premature infant with a C. parapsilosis blood infection revealed highly variable in situ expression patterns that are distinct from those of similar strains in pure cultures. For example, biofilm formation genes weremore »
- Authors:
-
[1];
[2];
[9]
- Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
- Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
- Stanford Univ. School of Medicine, CA (United States). Dept. of Microbiology and Immunology
- Chan Zuckerberg Biohub, San Francisco, CA (United States)
- Univ. of California, San Francisco, CA (United States). Dept. of Microbiology and Immunology
- Univ. of Pittsburgh School of Medicine, PA (United States). Dept. of Surgery
- Univ. of Pittsburgh School of Medicine, PA (United States). Magee-Womens Hospital, Division of Newborn Medicine
- Stanford Univ. School of Medicine, CA (United States). Dept. of Microbiology and Immunology; Univ. of California, San Francisco, CA (United States). Dept. of Microbiology and Immunology
- Chan Zuckerberg Biohub, San Francisco, CA (United States); Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy, and Management; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH); Alfred P. Sloan Foundation; National Science Foundation (NSF)
- OSTI Identifier:
- 1813128
- Grant/Contract Number:
- AC05-00OR22725; RAI092531A; APSF-2012- 10-05; DGE-1106400
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Microbial eukaryotes; Metagenomics; Genome-resolved metagenomics; Strain-tracking; Hospital microbiome; Neonatal intensive care unit; Premature infants; Candida
Citation Formats
West, Patrick T., Peters, Samantha L., Olm, Matthew R., Yu, Feiqiao B., Gause, Haley, Lou, Yue Clare, Firek, Brian A., Baker, Robyn, Johnson, Alexander D., Morowitz, Michael J., Hettich, Robert L., and Banfield, Jillian F. Genetic and behavioral adaptation of Candida parapsilosis to the microbiome of hospitalized infants revealed by in situ genomics, transcriptomics, and proteomics. United States: N. p., 2021.
Web. doi:10.1186/s40168-021-01085-y.
West, Patrick T., Peters, Samantha L., Olm, Matthew R., Yu, Feiqiao B., Gause, Haley, Lou, Yue Clare, Firek, Brian A., Baker, Robyn, Johnson, Alexander D., Morowitz, Michael J., Hettich, Robert L., & Banfield, Jillian F. Genetic and behavioral adaptation of Candida parapsilosis to the microbiome of hospitalized infants revealed by in situ genomics, transcriptomics, and proteomics. United States. https://doi.org/10.1186/s40168-021-01085-y
West, Patrick T., Peters, Samantha L., Olm, Matthew R., Yu, Feiqiao B., Gause, Haley, Lou, Yue Clare, Firek, Brian A., Baker, Robyn, Johnson, Alexander D., Morowitz, Michael J., Hettich, Robert L., and Banfield, Jillian F. Mon .
"Genetic and behavioral adaptation of Candida parapsilosis to the microbiome of hospitalized infants revealed by in situ genomics, transcriptomics, and proteomics". United States. https://doi.org/10.1186/s40168-021-01085-y. https://www.osti.gov/servlets/purl/1813128.
@article{osti_1813128,
title = {Genetic and behavioral adaptation of Candida parapsilosis to the microbiome of hospitalized infants revealed by in situ genomics, transcriptomics, and proteomics},
author = {West, Patrick T. and Peters, Samantha L. and Olm, Matthew R. and Yu, Feiqiao B. and Gause, Haley and Lou, Yue Clare and Firek, Brian A. and Baker, Robyn and Johnson, Alexander D. and Morowitz, Michael J. and Hettich, Robert L. and Banfield, Jillian F.},
abstractNote = {Background Candida parapsilosis is a common cause of invasive candidiasis, especially in newborn infants, and infections have been increasing over the past two decades. C. parapsilosis has been primarily studied in pure culture, leaving gaps in understanding of its function in a microbiome context. Results. Here, we compare five unique C. parapsilosis genomes assembled from premature infant fecal samples, three of which are newly reconstructed, and analyze their genome structure, population diversity, and in situ activity relative to reference strains in pure culture. All five genomes contain hotspots of single nucleotide variants, some of which are shared by strains from multiple hospitals. A subset of environmental and hospital-derived genomes share variants within these hotspots suggesting derivation of that region from a common ancestor. Four of the newly reconstructed C. parapsilosis genomes have 4 to 16 copies of the gene RTA3, which encodes a lipid translocase and is implicated in antifungal resistance, potentially indicating adaptation to hospital antifungal use. Time course metatranscriptomics and metaproteomics on fecal samples from a premature infant with a C. parapsilosis blood infection revealed highly variable in situ expression patterns that are distinct from those of similar strains in pure cultures. For example, biofilm formation genes were relatively less expressed in situ, whereas genes linked to oxygen utilization were more highly expressed, indicative of growth in a relatively aerobic environment. In gut microbiome samples, C. parapsilosis co-existed with Enterococcus faecalis that shifted in relative abundance over time, accompanied by changes in bacterial and fungal gene expression and proteome composition. Conclusions The results reveal potentially medically relevant differences in Candida function in gut vs. laboratory environments, and constrain evolutionary processes that could contribute to hospital strain persistence and transfer into premature infant microbiomes.},
doi = {10.1186/s40168-021-01085-y},
journal = {Microbiome},
number = 1,
volume = 9,
place = {United States},
year = {Mon Jun 21 00:00:00 EDT 2021},
month = {Mon Jun 21 00:00:00 EDT 2021}
}
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