Host DNA depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studies

Abstract Most respiratory microbiome studies use amplicon sequencing due to high host DNA. Metagenomics sequencing offers finer taxonomic resolution, phage assessment, and functional characterization. We evaluated five host DNA depletion methods on frozen nasal swabs from healthy adults, sputum from...

Full description

Saved in:
Bibliographic Details
Main Authors: Minsik Kim, Raymond C. Parrish, Michael J. Tisza, Viral S. Shah, Thi Tran, Matthew Ross, Juwan Cormier, Aribah Baig, Ching-Ying Huang, Laura Brenner, Isabel Neuringer, Katrine Whiteson, J. Kirk Harris, Amy D. Willis, Peggy S. Lai
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-07290-3
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846147509421867008
author Minsik Kim
Raymond C. Parrish
Michael J. Tisza
Viral S. Shah
Thi Tran
Matthew Ross
Juwan Cormier
Aribah Baig
Ching-Ying Huang
Laura Brenner
Isabel Neuringer
Katrine Whiteson
J. Kirk Harris
Amy D. Willis
Peggy S. Lai
author_facet Minsik Kim
Raymond C. Parrish
Michael J. Tisza
Viral S. Shah
Thi Tran
Matthew Ross
Juwan Cormier
Aribah Baig
Ching-Ying Huang
Laura Brenner
Isabel Neuringer
Katrine Whiteson
J. Kirk Harris
Amy D. Willis
Peggy S. Lai
author_sort Minsik Kim
collection DOAJ
description Abstract Most respiratory microbiome studies use amplicon sequencing due to high host DNA. Metagenomics sequencing offers finer taxonomic resolution, phage assessment, and functional characterization. We evaluated five host DNA depletion methods on frozen nasal swabs from healthy adults, sputum from people with cystic fibrosis (pwCF), and bronchoalveolar lavage (BAL) from critically ill patients. Median sequencing depth was 76.4 million reads per sample. Untreated nasal, sputum, and BAL had 94.1%, 99.2%, and 99.7% host reads, respectively. Host depletion effects varied by sample type, generally increasing microbial reads, species and functional richness; this was mediated by higher effective sequencing depth. Rarefaction curves showed species richness saturation at 0.5–2 million microbial reads. Most methods did not change Morisita-Horn dissimilarity for BAL and nasal samples although the proportion of gram-negative bacteria decreased for sputum from pwCF. Freezing did not affect the viability of Staphylococcus aureus but reduced the viability of Pseudomonas aeruginosa and Enterobacter spp.; this was mitigated by adding a cryoprotectant. QIAamp-based host depletion minimally impacted gram-negative viability even in non-cryoprotected frozen isolates. While some host depletion methods may shift microbial composition, metagenomics sequencing without host depletion severely underestimates microbial diversity of respiratory samples due to shallow effective sequencing depth and is not recommended.
format Article
id doaj-art-904329c9b9e5410ca04d6843f79769a1
institution Kabale University
issn 2399-3642
language English
publishDate 2024-11-01
publisher Nature Portfolio
record_format Article
series Communications Biology
spelling doaj-art-904329c9b9e5410ca04d6843f79769a12024-12-01T12:40:14ZengNature PortfolioCommunications Biology2399-36422024-11-017111510.1038/s42003-024-07290-3Host DNA depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studiesMinsik Kim0Raymond C. Parrish1Michael J. Tisza2Viral S. Shah3Thi Tran4Matthew Ross5Juwan Cormier6Aribah Baig7Ching-Ying Huang8Laura Brenner9Isabel Neuringer10Katrine Whiteson11J. Kirk Harris12Amy D. Willis13Peggy S. Lai14Division of Pulmonary and Critical Care Medicine, Massachusetts General HospitalDivision of Pulmonary and Critical Care Medicine, Massachusetts General HospitalAlkek Center for Metagenomics and Microbiome Research, Baylor College of MedicineDivision of Pulmonary and Critical Care Medicine, Massachusetts General HospitalDivision of Pulmonary and Critical Care Medicine, Massachusetts General HospitalAlkek Center for Metagenomics and Microbiome Research, Baylor College of MedicineAlkek Center for Metagenomics and Microbiome Research, Baylor College of MedicineDivision of Pulmonary and Critical Care Medicine, Massachusetts General HospitalDivision of Pulmonary and Critical Care Medicine, Massachusetts General HospitalDivision of Pulmonary and Critical Care Medicine, Massachusetts General HospitalDivision of Pulmonary and Critical Care Medicine, Massachusetts General HospitalDepartment of Molecular Biology & Biochemistry, University of California, IrvineDepartment of Pediatrics, University of Colorado Anschutz Medical CampusDepartment of Biostatistics, University of Washington School of Public HealthDivision of Pulmonary and Critical Care Medicine, Massachusetts General HospitalAbstract Most respiratory microbiome studies use amplicon sequencing due to high host DNA. Metagenomics sequencing offers finer taxonomic resolution, phage assessment, and functional characterization. We evaluated five host DNA depletion methods on frozen nasal swabs from healthy adults, sputum from people with cystic fibrosis (pwCF), and bronchoalveolar lavage (BAL) from critically ill patients. Median sequencing depth was 76.4 million reads per sample. Untreated nasal, sputum, and BAL had 94.1%, 99.2%, and 99.7% host reads, respectively. Host depletion effects varied by sample type, generally increasing microbial reads, species and functional richness; this was mediated by higher effective sequencing depth. Rarefaction curves showed species richness saturation at 0.5–2 million microbial reads. Most methods did not change Morisita-Horn dissimilarity for BAL and nasal samples although the proportion of gram-negative bacteria decreased for sputum from pwCF. Freezing did not affect the viability of Staphylococcus aureus but reduced the viability of Pseudomonas aeruginosa and Enterobacter spp.; this was mitigated by adding a cryoprotectant. QIAamp-based host depletion minimally impacted gram-negative viability even in non-cryoprotected frozen isolates. While some host depletion methods may shift microbial composition, metagenomics sequencing without host depletion severely underestimates microbial diversity of respiratory samples due to shallow effective sequencing depth and is not recommended.https://doi.org/10.1038/s42003-024-07290-3
spellingShingle Minsik Kim
Raymond C. Parrish
Michael J. Tisza
Viral S. Shah
Thi Tran
Matthew Ross
Juwan Cormier
Aribah Baig
Ching-Ying Huang
Laura Brenner
Isabel Neuringer
Katrine Whiteson
J. Kirk Harris
Amy D. Willis
Peggy S. Lai
Host DNA depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studies
Communications Biology
title Host DNA depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studies
title_full Host DNA depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studies
title_fullStr Host DNA depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studies
title_full_unstemmed Host DNA depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studies
title_short Host DNA depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studies
title_sort host dna depletion on frozen human respiratory samples enables successful metagenomic sequencing for microbiome studies
url https://doi.org/10.1038/s42003-024-07290-3
work_keys_str_mv AT minsikkim hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT raymondcparrish hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT michaeljtisza hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT viralsshah hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT thitran hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT matthewross hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT juwancormier hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT aribahbaig hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT chingyinghuang hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT laurabrenner hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT isabelneuringer hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT katrinewhiteson hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT jkirkharris hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT amydwillis hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies
AT peggyslai hostdnadepletiononfrozenhumanrespiratorysamplesenablessuccessfulmetagenomicsequencingformicrobiomestudies