Thousands of small, novel genes predicted in global phage genomes

Fremin, Brayon J.; Bhatt, Ami S.; Kyrpides, Nikos C.; Sengupta, Aditi; Sczyrba, Alexander; Maria da Silva, Aline; Buchan, Alison; Gaudin, Amelie; Brune, Andreas; Hirsch, Ann M.; Neumann, Anthony; Shade, Ashley; Visel, Axel; Campbell, Barbara; Baker, Brett; Hedlund, Brian P.; Crump, Byron C.; Currie, Cameron; Kelly, Charlene; Craft, Chris; Hazard, Christina; Francis, Christopher; Schadt, Christopher W.; Averill, Colin; Mobilian, Courtney; Buckley, Dan; Hunt, Dana; Noguera, Daniel; Beck, David; Valentine, David L.; Walsh, David; Sumner, Dawn; Lymperopoulou, Despoina; Bhaya, Devaki; Bryant, Donald A.; Morrison, Elise; Brodie, Eoin; Young, Erica; Lilleskov, Erik; Högfors-Rönnholm, Eva; Chen, Feng; Stewart, Frank; Nicol, Graeme W.; Teeling, Hanno; Beller, Harry R.; Dionisi, Hebe; Liao, Hui-Ling; Beman, J. Michael; Stegen, James; Tiedje, James; Jansson, Janet; VanderGheynst, Jean; Norton, Jeanette; Dangl, Jeff; Blanchard, Jeffrey; Bowen, Jennifer; Macalady, Jennifer; Pett-Ridge, Jennifer; Rich, Jeremy; Payet, Jérôme P.; Gladden, John D.; Raff, Jonathan D.; Klassen, Jonathan L.; Tarn, Jonathan; Neufeld, Josh; Gravuer, Kelly; Hofmockel, Kirsten; Chen, Ko-Hsuan; Konstantinidis, Konstantinos; DeAngelis, Kristen M.; Partida-Martinez, Laila P.; Meredith, Laura; Chistoserdova, Ludmila; Moran, Mary Ann; Scarborough, Matthew; Schrenk, Matthew; Sullivan, Matthew; David, Maude; O'Malley, Michelle A.; Medina, Monica; Habteselassie, Mussie; Ward, Nicholas D.; Pietrasiak, Nicole; Mason, Olivia U.; Sorensen, Patrick O.; Estrada de los Santos, Paulina; Baldrian, Petr; McKay, R. Michael; Simister, Rachel; Stepanauskas, Ramunas; Neumann, Rebecca; Malmstrom, Rex; Cavicchioli, Ricardo; Kelly, Robert; Hatzenpichler, Roland; Stocker, Roman; Cattolico, Rose Ann; Ziels, Ryan; Vilgalys, Rytas; Blumer-Schuette, Sara; Crowe, Sean; Roux, Simon; Hallam, Steven; Lindow, Steven; Brawley, Susan H.; Tringe, Susannah; Woyke, Tanja; Whitman, Thea; Bianchi, Thomas; Mock, Thomas; Donohue, Timothy; James, Timothy Y.; Kalluri, Udaya C.; Karaoz, Ulas; Denef, Vincent; Liu, Wen-Tso; Whitman, William; Ouyang, Yang

doi:10.1016/j.celrep.2022.110984

Thousands of small, novel genes predicted in global phage genomes

Journal Article · Tue Jun 21 00:00:00 EDT 2022 · Cell Reports

DOI:https://doi.org/10.1016/j.celrep.2022.110984· OSTI ID:1876276

^[1]; Bhatt, Ami S.; ; Sengupta, Aditi; Sczyrba, Alexander; Maria da Silva, Aline; Buchan, Alison; Gaudin, Amelie; Brune, Andreas; Hirsch, Ann M.; Neumann, Anthony; Shade, Ashley; Visel, Axel; Campbell, Barbara; Baker, Brett; Hedlund, Brian P.; Crump, Byron C.; Currie, Cameron; Kelly, Charlene; Craft, Chris more »

Joint Genome Institute, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); GP-SmORF Consortium. et al

We report 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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: National Institutes of Health (NIH); National Science Foundation (NSF); Simons Foundation; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

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

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725; AC52-07NA27344

OSTI ID:: 1876276

Alternate ID(s):: OSTI ID: 1889692
OSTI ID: 2565839
OSTI ID: 2583347

Report Number(s):: LLNL--JRNL-854337

Journal Information:: Cell Reports, Journal Name: Cell Reports Journal Issue: 12 Vol. 39; ISSN 2211-1247

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (74)

Differential effects of press vs. pulse seawater intrusion on microbial communities of a tidal freshwater marsh Mobilian, Courtney; Wisnoski, Nathan I.; Lennon, Jay T. Limnology and Oceanography Letters https://doi.org/10.1002/lol2.10171	journal	November 2020
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
Metagenomic Analysis of Subtidal Sediments from Polar and Subpolar Coastal Environments Highlights the Relevance of Anaerobic Hydrocarbon Degradation Processes Espínola, Fernando; Dionisi, Hebe M.; Borglin, Sharon Microbial Ecology, Vol. 75, Issue 1 https://doi.org/10.1007/s00248-017-1028-5	journal	July 2017
Molecular assembly and structure of the bacteriophage T4 tail Arisaka, Fumio; Yap, Moh Lan; Kanamaru, Shuji Biophysical Reviews, Vol. 8, Issue 4 https://doi.org/10.1007/s12551-016-0230-x	journal	November 2016
Dominance interactions in Escherichia coli cells mixedly infected with bacteriophage T4D wild-type and amber mutants and their possible implications as to type of gene-product function: Catalytic vs. stoichiometric Snustad, D. Peter Virology, Vol. 35, Issue 4 https://doi.org/10.1016/0042-6822(68)90285-7	journal	August 1968
Marine DNA Viral Macro- and Microdiversity from Pole to Pole Gregory, Ann C.; Zayed, Ahmed A.; Conceição-Neto, Nádia Cell, Vol. 177, Issue 5 https://doi.org/10.1016/j.cell.2019.03.040	journal	May 2019
The Gut Virome Database Reveals Age-Dependent Patterns of Virome Diversity in the Human Gut Gregory, Ann C.; Zablocki, Olivier; Zayed, Ahmed A. Cell Host & Microbe, Vol. 28, Issue 5 https://doi.org/10.1016/j.chom.2020.08.003	journal	November 2020
Automated Prediction and Annotation of Small Open Reading Frames in Microbial Genomes Durrant, Matthew G.; Bhatt, Ami S. Cell Host & Microbe, Vol. 29, Issue 1 https://doi.org/10.1016/j.chom.2020.11.002	journal	January 2021
Small bacterial and phagic proteins: an updated view on a rapidly moving field Duval, Mélodie; Cossart, Pascale Current Opinion in Microbiology, Vol. 39 https://doi.org/10.1016/j.mib.2017.09.010	journal	October 2017
Structure of the T4 baseplate and its function in triggering sheath contraction Taylor, Nicholas M. I.; Prokhorov, Nikolai S.; Guerrero-Ferreira, Ricardo C. Nature, Vol. 533, Issue 7603 https://doi.org/10.1038/nature17971	journal	May 2016
Uncovering Earth’s virome Paez-Espino, David; Eloe-Fadrosh, Emiley A.; Pavlopoulos, Georgios A. Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19094	journal	August 2016
Communication between viruses guides lysis–lysogeny decisions Erez, Zohar; Steinberger-Levy, Ida; Shamir, Maya Nature, Vol. 541, Issue 7638 https://doi.org/10.1038/nature21049	journal	January 2017
Strains, functions and dynamics in the expanded Human Microbiome Project Lloyd-Price, Jason; Mahurkar, Anup; Rahnavard, Gholamali Nature, Vol. 550, Issue 7674 https://doi.org/10.1038/nature23889	journal	September 2017
Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data Paez-Espino, David; Pavlopoulos, Georgios A.; Ivanova, Natalia N. Nature Protocols, Vol. 12, Issue 8 https://doi.org/10.1038/nprot.2017.063	journal	July 2017
Phages and their potential to modulate the microbiome and immunity Federici, Sara; Nobs, Samuel P.; Elinav, Eran Cellular & Molecular Immunology, Vol. 18, Issue 4 https://doi.org/10.1038/s41423-020-00532-4	journal	September 2020
Quorum sensing integrates environmental cues, cell density and cell history to control bacterial competence Moreno-Gámez, Stefany; Sorg, Robin A.; Domenech, Arnau Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00903-y	journal	October 2017
MetaRibo-Seq measures translation in microbiomes Fremin, Brayon J.; Sberro, Hila; Bhatt, Ami S. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17081-z	journal	June 2020
Energy efficiency and biological interactions define the core microbiome of deep oligotrophic groundwater Mehrshad, Maliheh; Lopez-Fernandez, Margarita; Sundh, John Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-24549-z	journal	July 2021
Host-linked soil viral ecology along a permafrost thaw gradient Emerson, Joanne B.; Roux, Simon; Brum, Jennifer R. Nature Microbiology, Vol. 3, Issue 8 https://doi.org/10.1038/s41564-018-0190-y	journal	July 2018
Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes Roux, Simon; Krupovic, Mart; Daly, Rebecca A. Nature Microbiology https://doi.org/10.1038/s41564-019-0510-x	journal	July 2019
Metagenomic compendium of 189,680 DNA viruses from the human gut microbiome Nayfach, Stephen; Páez-Espino, David; Call, Lee Nature Microbiology, Vol. 6, Issue 7 https://doi.org/10.1038/s41564-021-00928-6	journal	June 2021
Giant virus diversity and host interactions through global metagenomics Schulz, Frederik; Roux, Simon; Paez-Espino, David Nature, Vol. 578, Issue 7795 https://doi.org/10.1038/s41586-020-1957-x	journal	January 2020
SignalP 5.0 improves signal peptide predictions using deep neural networks Almagro Armenteros, José Juan; Tsirigos, Konstantinos D.; Sønderby, Casper Kaae Nature Biotechnology, Vol. 37, Issue 4 https://doi.org/10.1038/s41587-019-0036-z	journal	February 2019
A complete domain-to-species taxonomy for Bacteria and Archaea Parks, Donovan H.; Chuvochina, Maria; Chaumeil, Pierre-Alain Nature Biotechnology https://doi.org/10.1038/s41587-020-0501-8	journal	April 2020
Author Correction: A genomic catalog of Earth’s microbiomes Nayfach, Stephen; Roux, Simon; Seshadri, Rekha Nature Biotechnology, Vol. 39, Issue 4 https://doi.org/10.1038/s41587-021-00898-4	journal	April 2021
Simultaneous ribosome profiling of hundreds of microbes from the human microbiome Fremin, Brayon J.; Nicolaou, Cosmos; Bhatt, Ami S. Nature Protocols, Vol. 16, Issue 10 https://doi.org/10.1038/s41596-021-00592-4	journal	August 2021
AmPEP: Sequence-based prediction of antimicrobial peptides using distribution patterns of amino acid properties and random forest Bhadra, Pratiti; Yan, Jielu; Li, Jinyan Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-19752-w	journal	January 2018
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood Guindon, Stéphane; Gascuel, Olivier Systematic Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10635150390235520	journal	October 2003
Approximate Likelihood-Ratio Test for Branches: A Fast, Accurate, and Powerful Alternative Anisimova, Maria; Gascuel, Olivier Systematic Biology, Vol. 55, Issue 4 https://doi.org/10.1080/10635150600755453	journal	August 2006
VPF-Class: taxonomic assignment and host prediction of uncultivated viruses based on viral protein families Pons, Joan Carles; Paez-Espino, David; Riera, Gabriel Bioinformatics https://doi.org/10.1093/bioinformatics/btab026	journal	January 2021
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences Li, W.; Godzik, A. Bioinformatics, Vol. 22, Issue 13 https://doi.org/10.1093/bioinformatics/btl158	journal	May 2006
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
Gene and translation initiation site prediction in metagenomic sequences Hyatt, Doug; LoCascio, Philip F.; Hauser, Loren J. Bioinformatics, Vol. 28, Issue 17 https://doi.org/10.1093/bioinformatics/bts429	journal	July 2012
CD-HIT: accelerated for clustering the next-generation sequencing data Fu, Limin; Niu, Beifang; Zhu, Zhengwei Bioinformatics, Vol. 28, Issue 23 https://doi.org/10.1093/bioinformatics/bts565	journal	October 2012
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
RECODE: a database of frameshifting, bypassing and codon redefinition utilized for gene expression Baranov, P. V. Nucleic Acids Research, Vol. 29, Issue 1 https://doi.org/10.1093/nar/29.1.264	journal	January 2001
PaCRISPR: a server for predicting and visualizing anti-CRISPR proteins Wang, Jiawei; Dai, Wei; Li, Jiahui Nucleic Acids Research, Vol. 48, Issue W1 https://doi.org/10.1093/nar/gkaa432	journal	May 2020
AcrDB: a database of anti-CRISPR operons in prokaryotes and viruses Huang, Le; Yang, Bowen; Yi, Haidong Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa857	journal	October 2020
IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses Roux, Simon; Páez-Espino, David; Chen, I-Min A. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa946	journal	November 2020
AcrHub: an integrative hub for investigating, predicting and mapping anti-CRISPR proteins Wang, Jiawei; Dai, Wei; Li, Jiahui Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa951	journal	November 2020
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
CDD: a Conserved Domain Database for protein classification Marchler-Bauer, A. Nucleic Acids Research, Vol. 33, Issue Database issue https://doi.org/10.1093/nar/gki069	journal	December 2004
NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins Pruitt, K. D.; Tatusova, T.; Maglott, D. R. Nucleic Acids Research, Vol. 35, Issue Database https://doi.org/10.1093/nar/gkl842	journal	January 2007
Phylogeny.fr: robust phylogenetic analysis for the non-specialist Dereeper, A.; Guignon, V.; Blanc, G. Nucleic Acids Research, Vol. 36, Issue Web Server https://doi.org/10.1093/nar/gkn180	journal	May 2008
CDD: a Conserved Domain Database for the functional annotation of proteins Marchler-Bauer, A.; Lu, S.; Anderson, J. B. Nucleic Acids Research, Vol. 39, Issue Database https://doi.org/10.1093/nar/gkq1189	journal	November 2010
REPARATION: ribosome profiling assisted (re-)annotation of bacterial genomes Ndah, Elvis; Jonckheere, Veronique; Giess, Adam Nucleic Acids Research, Vol. 45, Issue 20 https://doi.org/10.1093/nar/gkx758	journal	August 2017
Genomes OnLine database (GOLD) v.7: updates and new features Mukherjee, Supratim; Stamatis, Dimitri; Bertsch, Jon Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky977	journal	October 2018
DeepRibo: a neural network for precise gene annotation of prokaryotes by combining ribosome profiling signal and binding site patterns Clauwaert, Jim; Menschaert, Gerben; Waegeman, Willem Nucleic Acids Research, Vol. 47, Issue 6 https://doi.org/10.1093/nar/gkz061	journal	February 2019
The EMBL-EBI search and sequence analysis tools APIs in 2019 Madeira, Fábio; Park, Young mi; Lee, Joon Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz268	journal	April 2019
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis Castresana, J. Molecular Biology and Evolution, Vol. 17, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a026334	journal	April 2000
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
A call for standardized classification of metagenome projects: Genomics update Ivanova, Natalia; Tringe, Susannah G.; Liolios, Konstantinos Environmental Microbiology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1462-2920.2010.02270.x	journal	March 2010
Uncovering small membrane proteins in pathogenic bacteria: Regulatory functions and therapeutic potential Garai, Preeti; Blanc‐Potard, Anne Molecular Microbiology, Vol. 114, Issue 5 https://doi.org/10.1111/mmi.14564	journal	July 2020
Genome-Wide Analysis in Vivo of Translation with Nucleotide Resolution Using Ribosome Profiling Ingolia, N. T.; Ghaemmaghami, S.; Newman, J. R. S. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1168978	journal	April 2009
Stop codon reassignments in the wild Ivanova, N. N.; Schwientek, P.; Tripp, H. J. Science, Vol. 344, Issue 6186, p. 909-913 https://doi.org/10.1126/science.1250691	journal	May 2014
Arginine-Rich Small Proteins with a Domain of Unknown Function, DUF1127, Play a Role in Phosphate and Carbon Metabolism of Agrobacterium tumefaciens Kraus, Alexander; Weskamp, Mareen; Zierles, Jennifer Journal of Bacteriology, Vol. 202, Issue 22 https://doi.org/10.1128/JB.00309-20	journal	October 2020
Draft Genome Sequence of Mn(II)-Oxidizing Bacterium Oxalobacteraceae sp. Strain AB_14 Bushman, Timothy J.; Akob, Denise M.; Bohu, Tsing Microbiology Resource Announcements, Vol. 8, Issue 43 https://doi.org/10.1128/MRA.01024-19	journal	October 2019
Structured RNA Contaminants in Bacterial Ribo-Seq Fremin, Brayon J.; Bhatt, Ami S. mSphere, Vol. 5, Issue 5 https://doi.org/10.1128/mSphere.00855-20	journal	October 2020
Bacterial Secretion Systems: An Overview Green, Erin R.; Mecsas, Joan Microbiology Spectrum, Vol. 4, Issue 1 https://doi.org/10.1128/microbiolspec.VMBF-0012-2015	journal	February 2016
Small Proteins Can No Longer Be Ignored Storz, Gisela; Wolf, Yuri I.; Ramamurthi, Kumaran S. Annual Review of Biochemistry, Vol. 83, Issue 1 https://doi.org/10.1146/annurev-biochem-070611-102400	journal	June 2014
Viral Miniproteins DiMaio, Daniel Annual Review of Microbiology, Vol. 68, Issue 1 https://doi.org/10.1146/annurev-micro-091313-103727	journal	September 2014
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
TreeDyn: towards dynamic graphics and annotations for analyses of trees Chevenet, François; Brun, Christine; Bañuls, Anne-Laure BMC Bioinformatics, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2105-7-439	journal	October 2006
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
The small protein floodgates are opening; now the functional analysis begins Ramamurthi, Kumaran S.; Storz, Gisela BMC Biology, Vol. 12, Issue 1 https://doi.org/10.1186/s12915-014-0096-y	journal	December 2014
VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data Ren, Jie; Ahlgren, Nathan A.; Lu, Yang Young Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0283-5	journal	July 2017
Diversity, evolution, and classification of virophages uncovered through global metagenomics Paez-Espino, David; Zhou, Jinglie; Roux, Simon Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0768-5	journal	December 2019
VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences Kieft, Kristopher; Zhou, Zhichao; Anantharaman, Karthik Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00867-0	journal	June 2020
RNAcode: Robust discrimination of coding and noncoding regions in comparative sequence data Washietl, S.; Findeiss, S.; Muller, S. A. RNA, Vol. 17, Issue 4 https://doi.org/10.1261/rna.2536111	journal	February 2011
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
Small proteins: untapped area of potential biological importance Su, Mingming; Ling, Yunchao; Yu, Jun Frontiers in Genetics, Vol. 4 https://doi.org/10.3389/fgene.2013.00286	journal	January 2013
Soil Microbes Trade-Off Biogeochemical Cycling for Stress Tolerance Traits in Response to Year-Round Climate Change Garcia, Maria O.; Templer, Pamela H.; Sorensen, Patrick O. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00616	journal	May 2020
A Primary Physiological Role of Toxin/Antitoxin Systems Is Phage Inhibition Song, Sooyeon; Wood, Thomas K. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01895	journal	August 2020
VirSorter: mining viral signal from microbial genomic data Roux, Simon; Enault, Francois; Hurwitz, Bonnie L. PeerJ, Vol. 3 https://doi.org/10.7717/peerj.985	journal	January 2015

Similar Records

Thousands of small, novel genes predicted in global phage genomes

Journal Article · Tue Jun 21 00:00:00 EDT 2022 · Cell Reports · OSTI ID:2565839

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
MetaRibo-Seq
comparative genomics
gene families
microbiome
phage
sORFs
small genes

Thousands of small, novel genes predicted in global phage genomes

Citation Formats

References (74)

Similar Records

Related Subjects