Resolving the structure of phage–bacteria interactions in the context of natural diversity

Kauffman, Kathryn M.; Chang, William K.; Brown, Julia M.; Hussain, Fatima A.; Yang, Joy; Polz, Martin F.; Kelly, Libusha

doi:10.1038/s41467-021-27583-z

Title: Resolving the structure of phage–bacteria interactions in the context of natural diversity

Journal Article · 17 January 2022 · Nature Communications

DOI: https://doi.org/10.1038/s41467-021-27583-z · OSTI ID:1904575

^[1]; Chang, William K. ^[2]; Brown, Julia M. ^[2];

^[3]; Yang, Joy ^[3];

^[4];

^[2]

Massachusetts Institute of Technology (MIT), Cambridge, MA (United States); Albert Einstein College of Medicine, Bronx, NY (United States)
Albert Einstein College of Medicine, Bronx, NY (United States)
Massachusetts Institute of Technology (MIT), Cambridge, MA (United States)
Massachusetts Institute of Technology (MIT), Cambridge, MA (United States); University of Vienna (Austria)

Microbial communities are shaped by viral predators. Yet, resolving which viruses (phages) and bacteria are interacting is a major challenge in the context of natural levels of microbial diversity. Thus, fundamental features of how phage-bacteria interactions are structured and evolve in the wild remain poorly resolved. Here we use large-scale isolation of environmental marine Vibrio bacteria and their phages to obtain estimates of strain-level phage predator loads, and use all-by-all host range assays to discover how phage and host genomic diversity shape interactions. We show that lytic interactions in environmental interaction networks (as observed in agar overlay) are sparse—with phage predator loads being low for most bacterial strains, and phages being host-strain-specific. Paradoxically, we also find that although overlap in killing is generally rare between tailed phages, recombination is common. Together, these results suggest that recombination during cryptic co-infections is an important mode of phage evolution in microbial communities. In the development of phages for bioengineering and therapeutics it is important to consider that nucleic acids of introduced phages may spread into local phage populations through recombination, and that the likelihood of transfer is not predictable based on lytic host range.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Krell Institute, Ames, IA (United States); Massachusetts Institute of Technology (MIT), Cambridge, MA (United States)

Sponsoring Organization:: National Science Foundation (NSF); Simons Foundation; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC); WHOI Ocean Ventures Fund

Grant/Contract Number:: FG02-97ER25308

OSTI ID:: 1904575

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 13; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (85)

BEDTools: The Swiss-Army Tool for Genome Feature Analysis: BEDTools: the Swiss-Army Tool for Genome Feature Analysis Quinlan, Aaron R. Current Protocols in Bioinformatics, Vol. 47, Issue 1 https://doi.org/10.1002/0471250953.bi1112s47	journal	September 2014
Answering biological questions by querying k‐mer databases Greenfield, Paul; Roehm, Uwe Concurrency and Computation: Practice and Experience, Vol. 25, Issue 4 https://doi.org/10.1002/cpe.2938	journal	October 2012
Awk — a pattern scanning and processing language Aho, Alfred V.; Kernighan, Brian W.; Weinberger, Peter J. Software: Practice and Experience, Vol. 9, Issue 4 https://doi.org/10.1002/spe.4380090403	journal	April 1979
Iron Chloride Flocculation of Bacteriophages from Seawater Poulos, Bonnie T.; John, Seth G.; Sullivan, Matthew B. Bacteriophages, p. 49-57 https://doi.org/10.1007/978-1-4939-7343-9_4	book	November 2017
Taxonomic investigations of bacteriophage sensitive bacteria isolated from marine waters Moebus, K.; Nattkemper, H. Helgoländer Meeresuntersuchungen, Vol. 36, Issue 4 https://doi.org/10.1007/BF01983456	journal	December 1983
Bacteriophage sensitivity patterns among bacteria isolated from marine waters Moebus, K.; Nattkemper, H. Helgoländer Meeresuntersuchungen, Vol. 34, Issue 3 https://doi.org/10.1007/BF02074130	journal	September 1981
Further investigations on the concentration of marine bacteriophages in the water around Helgoland, with reference to the phage-host systems encountered Moebus, K. Helgoländer Meeresuntersuchungen, Vol. 46, Issue 3 https://doi.org/10.1007/BF02367099	journal	September 1992
Meta-iPVP: a sequence-based meta-predictor for improving the prediction of phage virion proteins using effective feature representation Charoenkwan, Phasit; Nantasenamat, Chanin; Hasan, Md. Mehedi Journal of Computer-Aided Molecular Design, Vol. 34, Issue 10 https://doi.org/10.1007/s10822-020-00323-z	journal	June 2020
A Reverse Ecology Approach Based on a Biological Definition of Microbial Populations Arevalo, Philip; VanInsberghe, David; Elsherbini, Joseph Cell, Vol. 178, Issue 4 https://doi.org/10.1016/j.cell.2019.06.033	journal	August 2019
Probing Cellular Processes with Oligo-Mediated Recombination and Using the Knowledge Gained to Optimize Recombineering Sawitzke, James A.; Costantino, Nina; Li, Xin-tian Journal of Molecular Biology, Vol. 407, Issue 1, p. 45-59 https://doi.org/10.1016/j.jmb.2011.01.030	journal	March 2011
A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core Zimmermann, Lukas; Stephens, Andrew; Nam, Seung-Zin Journal of Molecular Biology, Vol. 430, Issue 15 https://doi.org/10.1016/j.jmb.2017.12.007	journal	July 2018
Streamlining standard bacteriophage methods for higher throughput Kauffman, Kathryn M.; Polz, Martin F. MethodsX, Vol. 5 https://doi.org/10.1016/j.mex.2018.01.007	journal	January 2018
Manipulating Bacterial Communities by in situ Microbiome Engineering Sheth, Ravi U.; Cabral, Vitor; Chen, Sway P. Trends in Genetics, Vol. 32, Issue 4 https://doi.org/10.1016/j.tig.2016.01.005	journal	April 2016
Phage–bacteria infection networks Weitz, Joshua S.; Poisot, Timothée; Meyer, Justin R. Trends in Microbiology, Vol. 21, Issue 2 https://doi.org/10.1016/j.tim.2012.11.003	journal	February 2013
HomBlocks: A multiple-alignment construction pipeline for organelle phylogenomics based on locally collinear block searching Bi, Guiqi; Mao, Yunxiang; Xing, Qikun Genomics, Vol. 110, Issue 1 https://doi.org/10.1016/j.ygeno.2017.08.001	journal	January 2018
A new logic for DNA engineering using recombination in Escherichia coli Zhang, Youming; Buchholz, Frank; Muyrers, Joep P. P. Nature Genetics, Vol. 20, Issue 2 https://doi.org/10.1038/2417	journal	October 1998
Recombineering: a powerful new tool for mouse functional genomics Copeland, Neal G.; Jenkins, Nancy A.; Court, Donald L. Nature Reviews Genetics, Vol. 2, Issue 10 https://doi.org/10.1038/35093556	journal	October 2001
Ecogenomics and genome landscapes of marine Pseudoalteromonas phage H105/1 Duhaime, Melissa Beth; Wichels, Antje; Waldmann, Jost The ISME Journal, Vol. 5, Issue 1 https://doi.org/10.1038/ismej.2010.94	journal	July 2010
Defining seasonal marine microbial community dynamics Gilbert, Jack A.; Steele, Joshua A.; Caporaso, J. Gregory The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.107	journal	August 2011
Reproducibility of Vibrionaceae population structure in coastal bacterioplankton Szabo, Gitta; Preheim, Sarah P.; Kauffman, Kathryn M. The ISME Journal, Vol. 7, Issue 3 https://doi.org/10.1038/ismej.2012.134	journal	November 2012
Multi-scale structure and geographic drivers of cross-infection within marine bacteria and phages Flores, Cesar O.; Valverde, Sergi; Weitz, Joshua S. The ISME Journal, Vol. 7, Issue 3 https://doi.org/10.1038/ismej.2012.135	journal	November 2012
Cyanophages infecting the oceanic cyanobacterium Prochlorococcus Sullivan, Matthew B.; Waterbury, John B.; Chisholm, Sallie W. Nature, Vol. 424, Issue 6952 https://doi.org/10.1038/nature01929	journal	August 2003
A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria Kauffman, Kathryn M.; Hussain, Fatima A.; Yang, Joy Nature, Vol. 554, Issue 7690 https://doi.org/10.1038/nature25474	journal	January 2018
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets Steinegger, Martin; Söding, Johannes Nature Biotechnology, Vol. 35, Issue 11 https://doi.org/10.1038/nbt.3988	journal	October 2017
The Phyre2 web portal for protein modeling, prediction and analysis Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M. Nature Protocols, Vol. 10, Issue 6 https://doi.org/10.1038/nprot.2015.053	journal	May 2015
Virulent coliphages in 1-year-old children fecal samples are fewer, but more infectious than temperate coliphages Mathieu, Aurélie; Dion, Moïra; Deng, Ling Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-14042-z	journal	January 2020
Flexible genes establish widespread bacteriophage pan-genomes in cryoconite hole ecosystems Bellas, Christopher M.; Schroeder, Declan C.; Edwards, Arwyn Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18236-8	journal	September 2020
The pan-immune system of bacteria: antiviral defence as a community resource Bernheim, Aude; Sorek, Rotem Nature Reviews Microbiology, Vol. 18, Issue 2 https://doi.org/10.1038/s41579-019-0278-2	journal	November 2019
Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks Bin Jang, Ho; Bolduc, Benjamin; Zablocki, Olivier Nature Biotechnology, Vol. 37, Issue 6 https://doi.org/10.1038/s41587-019-0100-8	journal	May 2019
Characterizing the portability of phage-encoded homologous recombination proteins Filsinger, Gabriel T.; Wannier, Timothy M.; Pedersen, Felix B. Nature Chemical Biology, Vol. 17, Issue 4 https://doi.org/10.1038/s41589-020-00710-5	journal	January 2021
Viruses of the Nahant Collection, characterization of 251 marine Vibrionaceae viruses Kauffman, Kathryn M.; Brown, Julia M.; Sharma, Radhey S. Scientific Data, Vol. 5, Issue 1 https://doi.org/10.1038/sdata.2018.114	journal	July 2018
Statistical structure of host-phage interactions Flores, C. O.; Meyer, J. R.; Valverde, S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 28 https://doi.org/10.1073/pnas.1101595108	journal	June 2011
Resistance in marine cyanobacteria differs against specialist and generalist cyanophages Zborowsky, Sophia; Lindell, Debbie Proceedings of the National Academy of Sciences, Vol. 116, Issue 34 https://doi.org/10.1073/pnas.1906897116	journal	August 2019
The lambda - P22 problem Ackermann, Hans-W Bacteriophage, Vol. 5, Issue 1 https://doi.org/10.1080/21597081.2015.1017084	journal	January 2015
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation Letunic, I.; Bork, P. Bioinformatics, Vol. 23, Issue 1 https://doi.org/10.1093/bioinformatics/btl529	journal	October 2006
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
BEDOPS: high-performance genomic feature operations Neph, Shane; Kuehn, M. Scott; Reynolds, Alex P. Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts277	journal	May 2012
InterProScan 5: genome-scale protein function classification Jones, P.; Binns, D.; Chang, H. -Y. Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu031	journal	January 2014
VICTOR: genome-based phylogeny and classification of prokaryotic viruses Meier-Kolthoff, Jan P.; Göker, Markus Bioinformatics, Vol. 33, Issue 21 https://doi.org/10.1093/bioinformatics/btx440	journal	July 2017
fastp: an ultra-fast all-in-one FASTQ preprocessor Chen, Shifu; Zhou, Yanqing; Chen, Yaru Bioinformatics, Vol. 34, Issue 17 https://doi.org/10.1093/bioinformatics/bty560	journal	September 2018
Twelve years of SAMtools and BCFtools Danecek, Petr; Bonfield, James K.; Liddle, Jennifer GigaScience, Vol. 10, Issue 2 https://doi.org/10.1093/gigascience/giab008	journal	January 2021
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper Huerta-Cepas, Jaime; Forslund, Kristoffer; Coelho, Luis Pedro Molecular Biology and Evolution, Vol. 34, Issue 8 https://doi.org/10.1093/molbev/msx148	journal	April 2017
Rates of Mutation and Recombination in Siphoviridae Phage Genome Evolution over Three Decades Kupczok, Anne; Neve, Horst; Huang, Kun D. Molecular Biology and Evolution, Vol. 35, Issue 5 https://doi.org/10.1093/molbev/msy027	journal	February 2018
Detection of novel recombinases in bacteriophage genomes unveils Rad52, Rad51 and Gp2.5 remote homologs Lopes, Anne; Amarir-Bouhram, Jihane; Faure, Guilhem Nucleic Acids Research, Vol. 38, Issue 12 https://doi.org/10.1093/nar/gkq096	journal	June 2010
Prokaryotic Virus Orthologous Groups (pVOGs): a resource for comparative genomics and protein family annotation Grazziotin, Ana Laura; Koonin, Eugene V.; Kristensen, David M. Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw975	journal	October 2016
eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses Huerta-Cepas, Jaime; Szklarczyk, Damian; Heller, Davide Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1085	journal	November 2018
Host-dependent differences in abundance, composition and host range of cyanophages from the Red Sea Dekel-Bird, Naama P.; Sabehi, Gazalah; Mosevitzky, Bar Environmental Microbiology, Vol. 17, Issue 4 https://doi.org/10.1111/1462-2920.12569	journal	August 2014
BiMat: a MATLAB package to facilitate the analysis of bipartite networks Flores, Cesar O.; Poisot, Timothée; Valverde, Sergi Methods in Ecology and Evolution, Vol. 7, Issue 1 https://doi.org/10.1111/2041-210X.12458	journal	August 2015
Metapopulation structure of Vibrionaceae among coastal marine invertebrates Preheim, Sarah P.; Boucher, Yan; Wildschutte, Hans Environmental Microbiology, Vol. 13, Issue 1 https://doi.org/10.1111/j.1462-2920.2010.02328.x	journal	September 2010
A simple and efficient method for concentration of ocean viruses by chemical flocculation: Virus concentration by flocculation with iron John, Seth G.; Mendez, Carolina B.; Deng, Li Environmental Microbiology Reports, Vol. 3, Issue 2 https://doi.org/10.1111/j.1758-2229.2010.00208.x	journal	August 2010
Genotypic Diversity Within a Natural Coastal Bacterioplankton Population Thompson, J. R. Science, Vol. 307, Issue 5713 https://doi.org/10.1126/science.1106028	journal	February 2005
Resource Partitioning and Sympatric Differentiation Among Closely Related Bacterioplankton Hunt, D. E.; David, L. A.; Gevers, D. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1157890	journal	May 2008
Systematic discovery of antiphage defense systems in the microbial pangenome Doron, Shany; Melamed, Sarah; Ofir, Gal Science, Vol. 359, Issue 6379 https://doi.org/10.1126/science.aar4120	journal	January 2018
Simple Method for Plating Escherichia coli Bacteriophages Forming Very Small Plaques or No Plaques under Standard Conditions Łoś, Joanna M.; Golec, Piotr; Węgrzyn, Grzegorz Applied and Environmental Microbiology, Vol. 74, Issue 16 https://doi.org/10.1128/AEM.00306-08	journal	August 2008
Evolution of a Vegetarian Vibrio: Metabolic Specialization of Vibrio breoganii to Macroalgal Substrates Corzett, Christopher H.; Elsherbini, Joseph; Chien, Diana M. Journal of Bacteriology, Vol. 200, Issue 15 https://doi.org/10.1128/JB.00020-18	journal	April 2018
Fluorescent Reporter DS6A Mycobacteriophages Reveal Unique Variations in Infectibility and Phage Production in Mycobacteria Mayer, Oren; Jain, Paras; Weisbrod, Torin R. Journal of Bacteriology, Vol. 198, Issue 23 https://doi.org/10.1128/JB.00592-16	journal	December 2016
Abortive Infection Mechanisms and Prophage Sequences Significantly Influence the Genetic Makeup of Emerging Lytic Lactococcal Phages Labrie, Simon J.; Moineau, Sylvain Journal of Bacteriology, Vol. 189, Issue 4 https://doi.org/10.1128/JB.01111-06	journal	February 2007
Use of Bacteriophage λ Recombination Functions To Promote Gene Replacement in Escherichia coli Murphy, Kenan C. Journal of Bacteriology, Vol. 180, Issue 8 https://doi.org/10.1128/JB.180.8.2063-2071.1998	journal	April 1998
Phage-Host Interaction: an Ecological Perspective Chibani-Chennoufi, S.; Bruttin, A.; Dillmann, M. -L. Journal of Bacteriology, Vol. 186, Issue 12 https://doi.org/10.1128/JB.186.12.3677-3686.2004	journal	June 2004
Resistance to Co-Occurring Phages Enables Marine Synechococcus Communities To Coexist with Cyanophages Abundant in Seawater † Waterbury, John B.; Valois, Frederica W. Applied and Environmental Microbiology, Vol. 59, Issue 10 https://doi.org/10.1128/aem.59.10.3393-3399.1993	journal	January 1993
HSP60 gene sequences as universal targets for microbial species identification: studies with coagulase-negative staphylococci Goh, S. H.; Potter, S.; Wood, J. O. Journal of Clinical Microbiology, Vol. 34, Issue 4 https://doi.org/10.1128/jcm.34.4.818-823.1996	journal	April 1996
Limitations of Correlation-Based Inference in Complex Virus-Microbe Communities Coenen, Ashley R.; Weitz, Joshua S. mSystems, Vol. 3, Issue 4 https://doi.org/10.1128/mSystems.00084-18	journal	August 2018
k -mer Similarity, Networks of Microbial Genomes, and Taxonomic Rank Bernard, Guillaume; Greenfield, Paul; Ragan, Mark A. mSystems, Vol. 3, Issue 6 https://doi.org/10.1128/mSystems.00257-18	journal	November 2018
MUSCLE: a multiple sequence alignment method with reduced time and space complexity Edgar, Robert C. BMC Bioinformatics, Vol. 5, Issue 1, p. 113 https://doi.org/10.1186/1471-2105-5-113	journal	August 2004
Automated classification of tailed bacteriophages according to their neck organization Lopes, Anne; Tavares, Paulo; Petit, Marie-Agnès BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-1027	journal	January 2014
The use of antibiotics to improve phage detection and enumeration by the double-layer agar technique Santos, Sílvio B.; Carvalho, Carla M.; Sillankorva, Sanna BMC Microbiology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2180-9-148	journal	July 2009
Mash: fast genome and metagenome distance estimation using MinHash Ondov, Brian D.; Treangen, Todd J.; Melsted, Páll Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-0997-x	journal	June 2016
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
ClonalFrameML: Efficient Inference of Recombination in Whole Bacterial Genomes Didelot, Xavier; Wilson, Daniel J. PLOS Computational Biology, Vol. 11, Issue 2 https://doi.org/10.1371/journal.pcbi.1004041	journal	February 2015
PhANNs, a fast and accurate tool and web server to classify phage structural proteins Cantu, Vito Adrian; Salamon, Peter; Seguritan, Victor PLOS Computational Biology, Vol. 16, Issue 11 https://doi.org/10.1371/journal.pcbi.1007845	journal	November 2020
The λ Red Proteins Promote Efficient Recombination between Diverged Sequences: Implications for Bacteriophage Genome Mosaicism Martinsohn, Jann T.; Radman, Miroslav; Petit, Marie-Agnès PLoS Genetics, Vol. 4, Issue 5 https://doi.org/10.1371/journal.pgen.1000065	journal	May 2008
Temperate Phages Acquire DNA from Defective Prophages by Relaxed Homologous Recombination: The Role of Rad52-Like Recombinases De Paepe, Marianne; Hutinet, Geoffrey; Son, Olivier PLoS Genetics, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pgen.1004181	journal	March 2014
Molecular Taxonomy of Phytopathogenic Fungi: A Case Study in Peronospora Göker, Markus; García-Blázquez, Gema; Voglmayr, Hermann PLoS ONE, Vol. 4, Issue 7 https://doi.org/10.1371/journal.pone.0006319	journal	July 2009
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement Darling, Aaron E.; Mau, Bob; Perna, Nicole T. PLoS ONE, Vol. 5, Issue 6 https://doi.org/10.1371/journal.pone.0011147	journal	June 2010
Agar Layer Method for Production of High Titer Phage Stocks. Swanstrom, M.; Adams, M. H. Experimental Biology and Medicine, Vol. 78, Issue 2 https://doi.org/10.3181/00379727-78-19076	journal	November 1951
Rates of Molecular Evolution in a Marine Synechococcus Phage Lineage Kupczok, Anne; Dagan, Tal Viruses, Vol. 11, Issue 8 https://doi.org/10.3390/v11080720	journal	August 2019
VIRIDIC—A Novel Tool to Calculate the Intergenomic Similarities of Prokaryote-Infecting Viruses Moraru, Cristina; Varsani, Arvind; Kropinski, Andrew M. Viruses, Vol. 12, Issue 11 https://doi.org/10.3390/v12111268	journal	November 2020
Understanding Bacteriophage Specificity in Natural Microbial Communities Koskella, Britt; Meaden, Sean Viruses, Vol. 5, Issue 3 https://doi.org/10.3390/v5030806	journal	March 2013
Mash: fast genome and metagenome distance estimation using MinHash Ondov, Brian; Treangen, Todd; Melsted, Pรกll Figshare https://doi.org/10.6084/m9.figshare.c.3635585	collection	January 2016
Viruses of the Nahant Collection, characterization of 251 marine Vibrionaceae viruses Kauffman, Kathryn M.; Brown, Julia Margaret; Shyam Sharma, Radhey figshare https://doi.org/10.6084/m9.figshare.c.4028239.v1	collection	January 2018
MetaCHIP: community-level horizontal gene transfer identification through the combination of best-match and phylogenetic approaches Song, Weizhi; Wemheuer, Bernd; Zhang, Shan figshare https://doi.org/10.6084/m9.figshare.c.4422620	collection	January 2019
FastViromeExplorer: a pipeline for virus and phage identification and abundance profiling in metagenomics data Tithi, Saima Sultana; Aylward, Frank O.; Jensen, Roderick V. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4227	journal	January 2018

Similar Records

High-throughput mapping of the phage resistance landscape in E. coli

Journal Article · 2020 · biorxiv.org Repository · OSTI ID:1609113

Mutalik, Vivek; Adler, Benjamin; Rishi, Harneet; +8 more

Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria

Journal Article · 2017 · Frontiers in Microbiology · OSTI ID:1524080

Gilbert, Rosalind A.; Kelly, William J.; Altermann, Eric; +4 more

Phage therapy: From biological mechanisms to future directions

Journal Article · 2023 · Cell · OSTI ID:1972189

Strathdee, Steffanie A.; Hatfull, Graham F.; Mutalik, Vivek K.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
bacteriophages
marine biology
microbial ecology

Title: Resolving the structure of phage–bacteria interactions in the context of natural diversity

Citation Formats

References (85)

Similar Records

Related Subjects