TY - JOUR
T1 - Resolving the structure of phage–bacteria interactions in the context of natural diversity
AU - Kauffman, Kathryn M.
AU - Chang, William K.
AU - Brown, Julia M.
AU - Hussain, Fatima A.
AU - Yang, Joy
AU - Polz, Martin F.
AU - Kelly, Libusha
N1 - Funding Information:
We are grateful to Jan Meier-Kolthoff and Markus Göker, for running their VICTOR tool analysis on the Nahant Collection phage genomes on their cluster. We thank Michael Cutler, Philip Arevalo, and Joseph Elsherbini for support in sequencing, assembly, and annotation of bacterial genomes. We thank David VanInsberghe for support in early phage genome analyses. We thank all members of the 2010 Polz lab for support with field sampling and bacterial isolation, and in particular Michael Cutler, Alison Takemura, Hong Xue, Tara Soni, and Gitta Szabo. We thank the Edward Ruby lab for sharing Vibrio fischeri strains for inclusion in the host range assay. This work was supported by grants from the National Science Foundation OCE 1435993 and 1435868 to M.P. and L.K., respectively, the Simons Foundation (LIFE ID 572792) to M.P., the NSF GRFP to F.H., and the WHOI Ocean Ventures Fund to K.K. J.Y. was supported by the Department of Energy Computational Science Graduate Fellowship Program of the Office of Science and National Nuclear Security Administration in the Department of Energy under contract DE-FG02-97ER25308.
Publisher Copyright:
© 2022, The Author(s).
PY - 2022/12
Y1 - 2022/12
N2 - 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.
AB - 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.
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U2 - 10.1038/s41467-021-27583-z
DO - 10.1038/s41467-021-27583-z
M3 - Article
C2 - 35042853
AN - SCOPUS:85123187869
SN - 2041-1723
VL - 13
JO - Nature Communications
JF - Nature Communications
IS - 1
M1 - 372
ER -