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Capturing sequence diversity in metagenomes with comprehensive and scalable probe design

Metagenomic sequencing has the potential to transform microbial detection and characterization, but new tools are needed to improve its sensitivity. Here we present CATCH, a computational method to enhance nucleic acid capture for enrichment of diverse microbial taxa. CATCH designs optimal probe set... Full description

Journal Title: Nature biotechnology 2019, Vol.37 (2), p.160-168
Main Author: Metsky, Hayden C
Other Authors: Siddle, Katherine J , Gladden-Young, Adrianne , Qu, James , Yang, David K , Brehio, Patrick , Goldfarb, Andrew , Piantadosi, Anne , Wohl, Shirlee , Carter, Amber , Lin, Aaron E , Barnes, Kayla G , Tully, Damien C , Corleis, Bjӧrn , Hennigan, Scott , Barbosa-Lima, Giselle , Vieira, Yasmine R , Paul, Lauren M , Tan, Amanda L , Garcia, Kimberly F , Parham, Leda A , Odia, Ikponmwosa , Eromon, Philomena , Folarin, Onikepe A , Goba, Augustine , Simon-Lorière, Etienne , Hensley, Lisa , Balmaseda, Angel , Harris, Eva , Kwon, Douglas S , Allen, Todd M , Runstadler, Jonathan A , Smole, Sandra , Bozza, Fernando A , Souza, Thiago M L , Isern, Sharon , Michael, Scott F , Lorenzana, Ivette , Gehrke, Lee , Bosch, Irene , Ebel, Gregory , Grant, Donald S , Happi, Christian T , Park, Daniel J , Gnirke, Andreas , Sabeti, Pardis C , Matranga, Christian B
Format: Electronic Article Electronic Article
Language: English
Subjects:
Publisher: United States: Nature Publishing Group
ID: ISSN: 1087-0156
Link: https://www.ncbi.nlm.nih.gov/pubmed/30718881
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title: Capturing sequence diversity in metagenomes with comprehensive and scalable probe design
format: Article
creator:
  • Metsky, Hayden C
  • Siddle, Katherine J
  • Gladden-Young, Adrianne
  • Qu, James
  • Yang, David K
  • Brehio, Patrick
  • Goldfarb, Andrew
  • Piantadosi, Anne
  • Wohl, Shirlee
  • Carter, Amber
  • Lin, Aaron E
  • Barnes, Kayla G
  • Tully, Damien C
  • Corleis, Bjӧrn
  • Hennigan, Scott
  • Barbosa-Lima, Giselle
  • Vieira, Yasmine R
  • Paul, Lauren M
  • Tan, Amanda L
  • Garcia, Kimberly F
  • Parham, Leda A
  • Odia, Ikponmwosa
  • Eromon, Philomena
  • Folarin, Onikepe A
  • Goba, Augustine
  • Simon-Lorière, Etienne
  • Hensley, Lisa
  • Balmaseda, Angel
  • Harris, Eva
  • Kwon, Douglas S
  • Allen, Todd M
  • Runstadler, Jonathan A
  • Smole, Sandra
  • Bozza, Fernando A
  • Souza, Thiago M L
  • Isern, Sharon
  • Michael, Scott F
  • Lorenzana, Ivette
  • Gehrke, Lee
  • Bosch, Irene
  • Ebel, Gregory
  • Grant, Donald S
  • Happi, Christian T
  • Park, Daniel J
  • Gnirke, Andreas
  • Sabeti, Pardis C
  • Matranga, Christian B
subjects:
  • Animals
  • Aquatic insects
  • Computational Biology - methods
  • Computer applications
  • Culicidae - virology
  • Disease Outbreaks
  • Enrichment
  • Fever
  • Gene Library
  • Genetic Variation
  • Genome, Viral
  • Genomes
  • Genomics
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Lassa fever
  • Lassa Fever - virology
  • Metagenome
  • Metagenomics
  • Microorganisms
  • Nigeria - epidemiology
  • Nucleic acids
  • Oligonucleotide Probes
  • Oligonucleotides
  • Oligonucleotides - genetics
  • Outbreaks
  • Sequence Analysis, DNA
  • Virus Diseases
ispartof: Nature biotechnology, 2019, Vol.37 (2), p.160-168
description: Metagenomic sequencing has the potential to transform microbial detection and characterization, but new tools are needed to improve its sensitivity. Here we present CATCH, a computational method to enhance nucleic acid capture for enrichment of diverse microbial taxa. CATCH designs optimal probe sets, with a specified number of oligonucleotides, that achieve full coverage of, and scale well with, known sequence diversity. We focus on applying CATCH to capture viral genomes in complex metagenomic samples. We design, synthesize, and validate multiple probe sets, including one that targets the whole genomes of the 356 viral species known to infect humans. Capture with these probe sets enriches unique viral content on average 18-fold, allowing us to assemble genomes that could not be recovered without enrichment, and accurately preserves within-sample diversity. We also use these probe sets to recover genomes from the 2018 Lassa fever outbreak in Nigeria and to improve detection of uncharacterized viral infections in human and mosquito samples. The results demonstrate that CATCH enables more sensitive and cost-effective metagenomic sequencing.
language: eng
source:
identifier: ISSN: 1087-0156
fulltext: no_fulltext
issn:
  • 1087-0156
  • 1546-1696
url: Link


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titleCapturing sequence diversity in metagenomes with comprehensive and scalable probe design
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creatorcontribMetsky, Hayden C ; Siddle, Katherine J ; Gladden-Young, Adrianne ; Qu, James ; Yang, David K ; Brehio, Patrick ; Goldfarb, Andrew ; Piantadosi, Anne ; Wohl, Shirlee ; Carter, Amber ; Lin, Aaron E ; Barnes, Kayla G ; Tully, Damien C ; Corleis, Bjӧrn ; Hennigan, Scott ; Barbosa-Lima, Giselle ; Vieira, Yasmine R ; Paul, Lauren M ; Tan, Amanda L ; Garcia, Kimberly F ; Parham, Leda A ; Odia, Ikponmwosa ; Eromon, Philomena ; Folarin, Onikepe A ; Goba, Augustine ; Simon-Lorière, Etienne ; Hensley, Lisa ; Balmaseda, Angel ; Harris, Eva ; Kwon, Douglas S ; Allen, Todd M ; Runstadler, Jonathan A ; Smole, Sandra ; Bozza, Fernando A ; Souza, Thiago M L ; Isern, Sharon ; Michael, Scott F ; Lorenzana, Ivette ; Gehrke, Lee ; Bosch, Irene ; Ebel, Gregory ; Grant, Donald S ; Happi, Christian T ; Park, Daniel J ; Gnirke, Andreas ; Sabeti, Pardis C ; Matranga, Christian B ; Viral Hemorrhagic Fever Consortium
descriptionMetagenomic sequencing has the potential to transform microbial detection and characterization, but new tools are needed to improve its sensitivity. Here we present CATCH, a computational method to enhance nucleic acid capture for enrichment of diverse microbial taxa. CATCH designs optimal probe sets, with a specified number of oligonucleotides, that achieve full coverage of, and scale well with, known sequence diversity. We focus on applying CATCH to capture viral genomes in complex metagenomic samples. We design, synthesize, and validate multiple probe sets, including one that targets the whole genomes of the 356 viral species known to infect humans. Capture with these probe sets enriches unique viral content on average 18-fold, allowing us to assemble genomes that could not be recovered without enrichment, and accurately preserves within-sample diversity. We also use these probe sets to recover genomes from the 2018 Lassa fever outbreak in Nigeria and to improve detection of uncharacterized viral infections in human and mosquito samples. The results demonstrate that CATCH enables more sensitive and cost-effective metagenomic sequencing.
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languageeng
publisherUnited States: Nature Publishing Group
subjectAnimals ; Aquatic insects ; Computational Biology - methods ; Computer applications ; Culicidae - virology ; Disease Outbreaks ; Enrichment ; Fever ; Gene Library ; Genetic Variation ; Genome, Viral ; Genomes ; Genomics ; High-Throughput Nucleotide Sequencing ; Humans ; Lassa fever ; Lassa Fever - virology ; Metagenome ; Metagenomics ; Microorganisms ; Nigeria - epidemiology ; Nucleic acids ; Oligonucleotide Probes ; Oligonucleotides ; Oligonucleotides - genetics ; Outbreaks ; Sequence Analysis, DNA ; Virus Diseases
ispartofNature biotechnology, 2019, Vol.37 (2), p.160-168
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8Wohl, Shirlee
9Carter, Amber
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12Tully, Damien C
13Corleis, Bjӧrn
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17Paul, Lauren M
18Tan, Amanda L
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20Parham, Leda A
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28Harris, Eva
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30Allen, Todd M
31Runstadler, Jonathan A
32Smole, Sandra
33Bozza, Fernando A
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35Isern, Sharon
36Michael, Scott F
37Lorenzana, Ivette
38Gehrke, Lee
39Bosch, Irene
40Ebel, Gregory
41Grant, Donald S
42Happi, Christian T
43Park, Daniel J
44Gnirke, Andreas
45Sabeti, Pardis C
46Matranga, Christian B
47Viral Hemorrhagic Fever Consortium
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descriptionMetagenomic sequencing has the potential to transform microbial detection and characterization, but new tools are needed to improve its sensitivity. Here we present CATCH, a computational method to enhance nucleic acid capture for enrichment of diverse microbial taxa. CATCH designs optimal probe sets, with a specified number of oligonucleotides, that achieve full coverage of, and scale well with, known sequence diversity. We focus on applying CATCH to capture viral genomes in complex metagenomic samples. We design, synthesize, and validate multiple probe sets, including one that targets the whole genomes of the 356 viral species known to infect humans. Capture with these probe sets enriches unique viral content on average 18-fold, allowing us to assemble genomes that could not be recovered without enrichment, and accurately preserves within-sample diversity. We also use these probe sets to recover genomes from the 2018 Lassa fever outbreak in Nigeria and to improve detection of uncharacterized viral infections in human and mosquito samples. The results demonstrate that CATCH enables more sensitive and cost-effective metagenomic sequencing.
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2Computational Biology - methods
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4Culicidae - virology
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10Genome, Viral
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8Wohl, Shirlee
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10Lin, Aaron E
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18Tan, Amanda L
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titleCapturing sequence diversity in metagenomes with comprehensive and scalable probe design
authorMetsky, Hayden C ; Siddle, Katherine J ; Gladden-Young, Adrianne ; Qu, James ; Yang, David K ; Brehio, Patrick ; Goldfarb, Andrew ; Piantadosi, Anne ; Wohl, Shirlee ; Carter, Amber ; Lin, Aaron E ; Barnes, Kayla G ; Tully, Damien C ; Corleis, Bjӧrn ; Hennigan, Scott ; Barbosa-Lima, Giselle ; Vieira, Yasmine R ; Paul, Lauren M ; Tan, Amanda L ; Garcia, Kimberly F ; Parham, Leda A ; Odia, Ikponmwosa ; Eromon, Philomena ; Folarin, Onikepe A ; Goba, Augustine ; Simon-Lorière, Etienne ; Hensley, Lisa ; Balmaseda, Angel ; Harris, Eva ; Kwon, Douglas S ; Allen, Todd M ; Runstadler, Jonathan A ; Smole, Sandra ; Bozza, Fernando A ; Souza, Thiago M L ; Isern, Sharon ; Michael, Scott F ; Lorenzana, Ivette ; Gehrke, Lee ; Bosch, Irene ; Ebel, Gregory ; Grant, Donald S ; Happi, Christian T ; Park, Daniel J ; Gnirke, Andreas ; Sabeti, Pardis C ; Matranga, Christian B
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8Gene Library
9Genetic Variation
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19Microorganisms
20Nigeria - epidemiology
21Nucleic acids
22Oligonucleotide Probes
23Oligonucleotides
24Oligonucleotides - genetics
25Outbreaks
26Sequence Analysis, DNA
27Virus Diseases
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2Gladden-Young, Adrianne
3Qu, James
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6Goldfarb, Andrew
7Piantadosi, Anne
8Wohl, Shirlee
9Carter, Amber
10Lin, Aaron E
11Barnes, Kayla G
12Tully, Damien C
13Corleis, Bjӧrn
14Hennigan, Scott
15Barbosa-Lima, Giselle
16Vieira, Yasmine R
17Paul, Lauren M
18Tan, Amanda L
19Garcia, Kimberly F
20Parham, Leda A
21Odia, Ikponmwosa
22Eromon, Philomena
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24Goba, Augustine
25Simon-Lorière, Etienne
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38Gehrke, Lee
39Bosch, Irene
40Ebel, Gregory
41Grant, Donald S
42Happi, Christian T
43Park, Daniel J
44Gnirke, Andreas
45Sabeti, Pardis C
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8Wohl, Shirlee
9Carter, Amber
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notes
0These authors contributed equally to this work.
1K.J.S, A.G.-Y., J.Q., and P.B. prepared samples, performed enrichment, and sequenced samples.
2E.S.-L. and L.H. shared viral seed stocks.
3K.J.S. and C.B.M. conceived of experimental design for evaluating probe sets.
4H.C.M., D.J.P., A.Gn., P.C.S., and C.B.M. initiated the study of improved design and application of comprehensive probe sets.
5I.O., P.E., O.A.F., A.Gob., D.S.G., and C.T.H. collected human plasma samples from Nigeria and Sierra Leone.
6These authors jointly supervised this work.
7C.B.M., J.Q., A.G.-Y., and K.J.S. developed enrichment protocols with help from A.Gol.
8G.E. shared uncharacterized mosquito pools.
9H.C.M. and K.J.S. formulated and performed data analyses with help from D.K.Y.
10D.C.T., B.C., S.H., G.B.-L., Y.R.V., L.M.P., A.L.T., K.F.G., L.A.P., A.B., E.H., D.S.K., T.M.A., J.A.R., S.S., F.A.B., T.M.L.S., S.I., S.F.M., I.L., L.G., and I.B. collected and shared samples with known viral content.
11H.C.M. conceived of CATCH and implemented it with advice from D.J.P., A.Gn., and C.B.M.
12A.P., S.W., A.C., A.E.L., and K.G.B. helped with sample preparation and enrichment.
13H.C.M., K.J.S., and C.B.M. wrote the manuscript with input from other authors.
14Author contributions
abstractMetagenomic sequencing has the potential to transform microbial detection and characterization, but new tools are needed to improve its sensitivity. Here we present CATCH, a computational method to enhance nucleic acid capture for enrichment of diverse microbial taxa. CATCH designs optimal probe sets, with a specified number of oligonucleotides, that achieve full coverage of, and scale well with, known sequence diversity. We focus on applying CATCH to capture viral genomes in complex metagenomic samples. We design, synthesize, and validate multiple probe sets, including one that targets the whole genomes of the 356 viral species known to infect humans. Capture with these probe sets enriches unique viral content on average 18-fold, allowing us to assemble genomes that could not be recovered without enrichment, and accurately preserves within-sample diversity. We also use these probe sets to recover genomes from the 2018 Lassa fever outbreak in Nigeria and to improve detection of uncharacterized viral infections in human and mosquito samples. The results demonstrate that CATCH enables more sensitive and cost-effective metagenomic sequencing.
copUnited States
pubNature Publishing Group
pmid30718881
doi10.1038/s41587-018-0006-x
tpages9
orcidid
0https://orcid.org/0000-0002-9972-3035
1https://orcid.org/0000-0001-7400-4125
2https://orcid.org/0000-0002-4329-0795
3https://orcid.org/0000-0002-8871-2349
4https://orcid.org/0000-0001-5503-7570
oafree_for_read