Thousands of small, novel genes predicted in global phage genomes

Global Phage Small Open Reading Frame (GP-SmORF) Consortium

doi:10.1016/j.celrep.2022.110984

Thousands of small, novel genes predicted in global phage genomes

Global Phage Small Open Reading Frame (GP-SmORF) Consortium

Research output: Contribution to journal › Article › peer-review

25 Scopus citations

Abstract

Small genes (<150 nucleotides) have been systematically overlooked in phage genomes. We employ a large-scale comparative genomics approach to predict >40,000 small-gene families in ∼2.3 million phage genome contigs. We find that small genes in phage genomes are approximately 3-fold more prevalent than in host prokaryotic genomes. Our approach enriches for small genes that are translated in microbiomes, suggesting the small genes identified are coding. More than 9,000 families encode potentially secreted or transmembrane proteins, more than 5,000 families encode predicted anti-CRISPR proteins, and more than 500 families encode predicted antimicrobial proteins. By combining homology and genomic-neighborhood analyses, we reveal substantial novelty and diversity within phage biology, including small phage genes found in multiple host phyla, small genes encoding proteins that play essential roles in host infection, and small genes that share genomic neighborhoods and whose encoded proteins may share related functions.

Original language	English
Article number	110984
Journal	Cell Reports
Volume	39
Issue number	12
DOIs	https://doi.org/10.1016/j.celrep.2022.110984
State	Published - Jun 21 2022

Funding

We would like to thank Stephen Nayfach for help in identifying resources and suggesting ideas to enhance the manuscript. We also thank Heather Maughan for critical reading of the manuscript. We thank Timothy James for feedback on the manuscript. The work conducted by the U.S. Department of Energy Joint Genome Institute , a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under contract no. DE-AC02-05CH11231 . Computing costs were also supported via NIH S10 Shared Instrumentation Grant ( 1S10OD02014101 ), NIH R01 #AI148623–01 , A Sloan Foundation Fellowship, and Damon Runyon Clinical Investigator Award to A.S.B. Sample collection costs were supported by NSF grants 1826734 and 1441717 as well as Simons Foundation grant 827839 .

Keywords

CP: Microbiology
MetaRibo-Seq
comparative genomics
gene families
microbiome
phage
sORFs
small genes

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10.1016/j.celrep.2022.110984

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title = "Thousands of small, novel genes predicted in global phage genomes",

abstract = "Small genes (<150 nucleotides) have been systematically overlooked in phage genomes. We employ a large-scale comparative genomics approach to predict >40,000 small-gene families in ∼2.3 million phage genome contigs. We find that small genes in phage genomes are approximately 3-fold more prevalent than in host prokaryotic genomes. Our approach enriches for small genes that are translated in microbiomes, suggesting the small genes identified are coding. More than 9,000 families encode potentially secreted or transmembrane proteins, more than 5,000 families encode predicted anti-CRISPR proteins, and more than 500 families encode predicted antimicrobial proteins. By combining homology and genomic-neighborhood analyses, we reveal substantial novelty and diversity within phage biology, including small phage genes found in multiple host phyla, small genes encoding proteins that play essential roles in host infection, and small genes that share genomic neighborhoods and whose encoded proteins may share related functions.",

keywords = "CP: Microbiology, MetaRibo-Seq, comparative genomics, gene families, microbiome, phage, sORFs, small genes",

author = "{Global Phage Small Open Reading Frame (GP-SmORF) Consortium} and Fremin, {Brayon J.} and Bhatt, {Ami S.} and Kyrpides, {Nikos C.} and Aditi Sengupta and Alexander Sczyrba and {Maria da Silva}, Aline and Alison Buchan and Amelie Gaudin and Andreas Brune and Hirsch, {Ann M.} and Anthony Neumann and Ashley Shade and Axel Visel and Barbara Campbell and Brett Baker and Hedlund, {Brian P.} and Crump, {Byron C.} and Cameron Currie and Charlene Kelly and Chris Craft and Christina Hazard and Christopher Francis and Schadt, {Christopher W.} and Colin Averill and Courtney Mobilian and Dan Buckley and Dana Hunt and Daniel Noguera and David Beck and Valentine, {David L.} and David Walsh and Dawn Sumner and Despoina Lymperopoulou and Devaki Bhaya and Bryant, {Donald A.} and Elise Morrison and Eoin Brodie and Erica Young and Erik Lilleskov and Eva H{\"o}gfors-R{\"o}nnholm and Feng Chen and Frank Stewart and Nicol, {Graeme W.} and Hanno Teeling and Beller, {Harry R.} and Hebe Dionisi and Liao, {Hui Ling} and Beman, {J. Michael} and James Stegen and Kalluri, {Udaya C.}",

note = "Publisher Copyright: {\textcopyright} 2022",

year = "2022",

month = jun,

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doi = "10.1016/j.celrep.2022.110984",

language = "English",

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AU - Fremin, Brayon J.

AU - Bhatt, Ami S.

AU - Kyrpides, Nikos C.

AU - Sengupta, Aditi

AU - Sczyrba, Alexander

AU - Maria da Silva, Aline

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AU - Gaudin, Amelie

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AU - Hirsch, Ann M.

AU - Neumann, Anthony

AU - Shade, Ashley

AU - Visel, Axel

AU - Campbell, Barbara

AU - Baker, Brett

AU - Hedlund, Brian P.

AU - Crump, Byron C.

AU - Currie, Cameron

AU - Kelly, Charlene

AU - Craft, Chris

AU - Hazard, Christina

AU - Francis, Christopher

AU - Schadt, Christopher W.

AU - Averill, Colin

AU - Mobilian, Courtney

AU - Buckley, Dan

AU - Hunt, Dana

AU - Noguera, Daniel

AU - Beck, David

AU - Valentine, David L.

AU - Walsh, David

AU - Sumner, Dawn

AU - Lymperopoulou, Despoina

AU - Bhaya, Devaki

AU - Bryant, Donald A.

AU - Morrison, Elise

AU - Brodie, Eoin

AU - Young, Erica

AU - Lilleskov, Erik

AU - Högfors-Rönnholm, Eva

AU - Chen, Feng

AU - Stewart, Frank

AU - Nicol, Graeme W.

AU - Teeling, Hanno

AU - Beller, Harry R.

AU - Dionisi, Hebe

AU - Liao, Hui Ling

AU - Beman, J. Michael

AU - Stegen, James

AU - Kalluri, Udaya C.

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AB - Small genes (<150 nucleotides) have been systematically overlooked in phage genomes. We employ a large-scale comparative genomics approach to predict >40,000 small-gene families in ∼2.3 million phage genome contigs. We find that small genes in phage genomes are approximately 3-fold more prevalent than in host prokaryotic genomes. Our approach enriches for small genes that are translated in microbiomes, suggesting the small genes identified are coding. More than 9,000 families encode potentially secreted or transmembrane proteins, more than 5,000 families encode predicted anti-CRISPR proteins, and more than 500 families encode predicted antimicrobial proteins. By combining homology and genomic-neighborhood analyses, we reveal substantial novelty and diversity within phage biology, including small phage genes found in multiple host phyla, small genes encoding proteins that play essential roles in host infection, and small genes that share genomic neighborhoods and whose encoded proteins may share related functions.

KW - CP: Microbiology

KW - MetaRibo-Seq

KW - comparative genomics

KW - gene families

KW - microbiome

KW - phage

KW - sORFs

KW - small genes

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C2 - 35732113

AN - SCOPUS:85132618487

SN - 2211-1247

VL - 39

JO - Cell Reports

JF - Cell Reports

IS - 12

M1 - 110984

ER -

Thousands of small, novel genes predicted in global phage genomes

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