Tapping the treasure trove of atypical phages

Roux, Simon; Mutalik, Vivek K.

doi:10.1016/j.mib.2024.102555

Title: Tapping the treasure trove of atypical phages

Journal Article · 10 October 2024 · Current Opinion in Microbiology

DOI: https://doi.org/10.1016/j.mib.2024.102555 · OSTI ID:2477758

Roux, Simon ^[1];

^[1]

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

With advancements in genomics technologies, a vast diversity of ‘atypical’ phages, that is, with single-stranded DNA or RNA genomes, are being uncovered from different ecosystems. Though these efforts have revealed the existence and prevalence of these nonmodel phages, computational approaches often fail to associate these phages with their specific bacterial host(s), while the lack of methods to isolate these phages has limited our ability to characterize infectivity pathways and new gene function. In this review, we call for the development of generalizable experimental methods to better capture this understudied viral diversity via isolation and study them through gene-level characterization and engineering. Establishing a diverse set of new ‘atypical’ phage model systems has the potential to provide many new biotechnologies, including potential uses of these atypical phages in halting the spread of antibiotic resistance and engineering of microbial communities for beneficial outcomes.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2477758

Journal Information:: Current Opinion in Microbiology, Journal Name: Current Opinion in Microbiology Vol. 82; ISSN 1369-5274

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (45)

Effect of RNase pre-treatment of cells of Escherichia coli K 12 on plaque yields resulting from subsequent infection with the RNA phage fr+ Knolle, P.; Kaudewitz, F. Biochemical and Biophysical Research Communications, Vol. 11, Issue 5 https://doi.org/10.1016/0006-291X(63)90127-X	journal	May 1963
The F-Pilus of Escherichia coli Valentine, Raymond C.; Silverman, P. M.; Ippen, K. A. Advances in Microbial Physiology https://doi.org/10.1016/S0065-2911(08)60364-1	book	January 1969
Characterization of filamentous phages of Vibrio cholerae O139 and O1 Ehara, M. FEMS Microbiology Letters, Vol. 154, Issue 2 https://doi.org/10.1016/S0378-1097(97)00345-5	journal	September 1997
Expansion of the global RNA virome reveals diverse clades of bacteriophages Neri, Uri; Wolf, Yuri I.; Roux, Simon Cell, Vol. 185, Issue 21 https://doi.org/10.1016/j.cell.2022.08.023	journal	October 2022
Filamentous Bacteriophage Promote Biofilm Assembly and Function Secor, Patrick R.; Sweere, Johanna M.; Michaels, Lia A. Cell Host & Microbe, Vol. 18, Issue 5 https://doi.org/10.1016/j.chom.2015.10.013	journal	November 2015
F conjugation: Back to the beginning Arutyunov, Denis; Frost, Laura S. Plasmid, Vol. 70, Issue 1 https://doi.org/10.1016/j.plasmid.2013.03.010	journal	July 2013
A review on pilus assembly mechanisms in Gram-positive and Gram-negative bacteria Shanmugasundarasamy, Tamilarasi; Karaiyagowder Govindarajan, Deenadayalan; Kandaswamy, Kumaravel The Cell Surface, Vol. 8 https://doi.org/10.1016/j.tcsw.2022.100077	journal	December 2022
Pili in Gram-positive pathogens Telford, John L.; Barocchi, Michèle A.; Margarit, Immaculada Nature Reviews Microbiology, Vol. 4, Issue 7 https://doi.org/10.1038/nrmicro1443	journal	July 2006
Marine viruses — major players in the global ecosystem Suttle, Curtis A. Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1750	journal	October 2007
Structural basis for the adsorption of a single-stranded RNA bacteriophage Meng, Ran; Jiang, Mengqiu; Cui, Zhicheng Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11126-8	journal	July 2019
PHEIGES: all-cell-free phage synthesis and selection from engineered genomes Levrier, Antoine; Karpathakis, Ioannis; Nash, Bruce Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-46585-1	journal	March 2024
Diverse and abundant phages exploit conjugative plasmids Quinones-Olvera, Natalia; Owen, Siân V.; McCully, Lucy M. Nature Communications, Vol. 15, Issue 1 https://doi.org/10.1038/s41467-024-47416-z	journal	April 2024
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
Interactions between bacterial and phage communities in natural environments Chevallereau, Anne; Pons, Benoît J.; van Houte, Stineke Nature Reviews Microbiology, Vol. 20, Issue 1 https://doi.org/10.1038/s41579-021-00602-y	journal	August 2021
Structural and functional diversity of type IV secretion systems Costa, Tiago R. D.; Patkowski, Jonasz B.; Macé, Kévin Nature Reviews Microbiology, Vol. 22, Issue 3 https://doi.org/10.1038/s41579-023-00974-3	journal	October 2023
Multicopy suppressor screens reveal convergent evolution of single-gene lysis proteins Adler, Benjamin A.; Chamakura, Karthik; Carion, Heloise Nature Chemical Biology, Vol. 19, Issue 6 https://doi.org/10.1038/s41589-023-01269-7	journal	February 2023
Geochemical constraints on bacteriophage infectivity in terrestrial environments Carlson, Hans K.; Piya, Denish; Moore, Madeline L. ISME Communications, Vol. 3, Issue 1 https://doi.org/10.1038/s43705-023-00297-7	journal	August 2023
The Isolation and Oharacterization of An Rna Bacteriophage Davern, Ci Australian Journal of Biological Sciences, Vol. 17, Issue 3 https://doi.org/10.1071/BI9640719	journal	January 1964
Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil Starr, Evan P.; Nuccio, Erin E.; Pett-Ridge, Jennifer Proceedings of the National Academy of Sciences, Vol. 116, Issue 51 https://doi.org/10.1073/pnas.1908291116	journal	November 2019
ssRNA phage penetration triggers detachment of the F-pilus Harb, Laith; Chamakura, Karthik; Khara, Pratick Proceedings of the National Academy of Sciences, Vol. 117, Issue 41 https://doi.org/10.1073/pnas.2011901117	journal	September 2020
Phage single-gene lysis: Finding the weak spot in the bacterial cell wall Chamakura, Karthik; Young, Ry Journal of Biological Chemistry, Vol. 294, Issue 10 https://doi.org/10.1074/jbc.TM118.001773	journal	November 2018
Single-stranded DNA phages: from early molecular biology tools to recent revolutions in environmental microbiology Székely, Anna J.; Breitbart, Mya FEMS Microbiology Letters, Vol. 363, Issue 6 https://doi.org/10.1093/femsle/fnw027	journal	February 2016
‘Big things in small packages: the genetics of filamentous phage and effects on fitness of their host’ Mai-Prochnow, Anne; Hui, Janice Gee Kay; Kjelleberg, Staffan FEMS Microbiology Reviews, Vol. 39, Issue 4 https://doi.org/10.1093/femsre/fuu007	journal	February 2015
IMG/VR v4: an expanded database of uncultivated virus genomes within a framework of extensive functional, taxonomic, and ecological metadata Camargo, Antonio Pedro; Nayfach, Stephen; Chen, I-Min A. Nucleic Acids Research, Vol. 51, Issue D1 https://doi.org/10.1093/nar/gkac1037	journal	November 2022
Black box of phage–bacterium interactions: exploring alternative phage infection strategies Mäntynen, Sari; Laanto, Elina; Oksanen, Hanna M. Open Biology, Vol. 11, Issue 9 https://doi.org/10.1098/rsob.210188	journal	September 2021
Structure, Biology, and Applications of Filamentous Bacteriophages Rakonjac, Jasna; Gold, Vicki A. M.; León-Quezada, Rayén I. Cold Spring Harbor Protocols, Vol. 2024, Issue 8 https://doi.org/10.1101/pdb.over107754	journal	July 2023
A Review: The isolation of bacteriophages from the environment Seeley, N. D.; Primrose, S. B. Journal of Applied Bacteriology, Vol. 53, Issue 1 https://doi.org/10.1111/j.1365-2672.1982.tb04729.x	journal	August 1982
Pretreatment to reduce somatic salmonella phage interference with FRNA coliphage assays: successful use in a one-year survey of vulnerable groundwaters Stetler, R. E.; Jr, F. P. Williams Letters in Applied Microbiology, Vol. 23, Issue 1 https://doi.org/10.1111/j.1472-765X.1996.tb00027.x	journal	July 1996
Expansion of known ssRNA phage genomes: From tens to over a thousand Callanan, J.; Stockdale, S. R.; Shkoporov, A. Science Advances, Vol. 6, Issue 6 https://doi.org/10.1126/sciadv.aay5981	journal	February 2020
Isolation of Additional Bacteriophages with Genomes of Segmented Double-Stranded RNA Mindich, Leonard; Qiao, Xueying; Qiao, Jian Journal of Bacteriology, Vol. 181, Issue 15 https://doi.org/10.1128/JB.181.15.4505-4508.1999	journal	August 1999
Gene Mapping and Phylogenetic Analysis of the Complete Genome from 30 Single-Stranded RNA Male-Specific Coliphages (Family Leviviridae ) Friedman, Stephanie D.; Genthner, Fred J.; Gentry, Jennifer Journal of Virology, Vol. 83, Issue 21 https://doi.org/10.1128/JVI.01308-09	journal	November 2009
Methods for Studying Aquatic Bacteriophage Ecology Primrose, Sandy B.; Seeley, Nigel D.; Logan, Kelvin B. Applied and Environmental Microbiology, Vol. 43, Issue 3 https://doi.org/10.1128/aem.43.3.694-701.1982	journal	March 1982
The True Story and Advantages of RNA Phage Capsids as Nanotools Pumpens, Paul; Renhofa, Regina; Dishlers, Andris Intervirology, Vol. 59, Issue 2 https://doi.org/10.1159/000449503	journal	January 2016
Production and characterization of novel ssRNA bacteriophage virus-like particles from metagenomic sequencing data Liekniņa, Ilva; Kalniņš, Gints; Akopjana, Ināra Journal of Nanobiotechnology, Vol. 17, Issue 1 https://doi.org/10.1186/s12951-019-0497-8	journal	May 2019
Gut commensal Enterocloster species host inoviruses that are secreted in vitro and in vivo Burckhardt, Juan C.; Chong, Derrick H. Y.; Pett, Nicola Microbiome, Vol. 11, Issue 1 https://doi.org/10.1186/s40168-023-01496-z	journal	March 2023
Single-stranded RNA phages: From molecular biology to nanotechnology Pumpens, Paul https://doi.org/10.1201/9780429001208	book	January 2020
Hyperexpansion of RNA Bacteriophage Diversity Krishnamurthy, Siddharth R.; Janowski, Andrew B.; Zhao, Guoyan PLOS Biology, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pbio.1002409	journal	March 2016
High-throughput mapping of the phage resistance landscape in E. coli Mutalik, Vivek K.; Adler, Benjamin A.; Rishi, Harneet S. PLOS Biology, Vol. 18, Issue 10 https://doi.org/10.1371/journal.pbio.3000877	journal	October 2020
Systematic and scalable genome-wide essentiality mapping to identify nonessential genes in phages Piya, Denish; Nolan, Nicholas; Moore, Madeline L. PLOS Biology, Vol. 21, Issue 12 https://doi.org/10.1371/journal.pbio.3002416	journal	December 2023
From conjugation to T4S systems in Gram‐negative bacteria: a mechanistic biology perspective Waksman, Gabriel EMBO reports, Vol. 20, Issue 2 https://doi.org/10.15252/embr.201847012	journal	January 2019
Filamentous phages: masters of a microbial sharing economy Hay, Iain D.; Lithgow, Trevor EMBO reports, Vol. 20, Issue 6 https://doi.org/10.15252/embr.201847427	journal	April 2019
RNA and Single-Stranded DNA Phages: Unveiling the Promise from the Underexplored World of Viruses Nguyen, Huong Minh; Watanabe, Shinya; Sharmin, Sultana International Journal of Molecular Sciences, Vol. 24, Issue 23 https://doi.org/10.3390/ijms242317029	journal	December 2023
RNA Phage Biology in a Metagenomic Era Callanan, Julie; Stockdale, Stephen; Shkoporov, Andrey Viruses, Vol. 10, Issue 7 https://doi.org/10.3390/v10070386	journal	July 2018
Filamentous Pseudomonas Phage Pf4 in the Context of Therapy-Inducibility, Infectivity, Lysogenic Conversion, and Potential Application Gavric, Damir; Knezevic, Petar Viruses, Vol. 14, Issue 6 https://doi.org/10.3390/v14061261	journal	June 2022
Recent Advances in Structural Studies of Single-Stranded RNA Bacteriophages Thongchol, Jirapat; Lill, Zachary; Hoover, Zachary Viruses, Vol. 15, Issue 10 https://doi.org/10.3390/v15101985	journal	September 2023

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