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  • Review Article
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Phage puppet masters of the marine microbial realm

Nature Microbiology volume 3, pages 754–766 (2018)Cite this article

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Abstract

Viruses numerically dominate our oceans; however, we have only just begun to document the diversity, host range and infection dynamics of marine viruses, as well as the subsequent effects of infection on both host cell metabolism and oceanic biogeochemistry. Bacteriophages (that is, phages: viruses that infect bacteria) are highly abundant and are known to play critical roles in bacterial mortality, biogeochemical cycling and horizontal gene transfer. This Review Article summarizes current knowledge of marine viral ecology and highlights the importance of phage particles to the dissolved organic matter pool, as well as the complex interactions between phages and their bacterial hosts. We emphasize the newly recognized roles of phages as puppet masters of their bacterial hosts, where phages are capable of altering the metabolism of infected bacteria through the expression of auxiliary metabolic genes and the redirection of host gene expression patterns. Finally, we propose the ‘royal family model’ as a hypothesis to describe successional patterns of bacteria and phages over time in marine systems, where despite high richness and significant seasonal differences, only a small number of phages appear to continually dominate a given marine ecosystem. Although further testing is required, this model provides a framework for assessing the specificity and ecological consequences of phage–host dynamics.

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Fig. 1: The size of biology in the oceans spans nine orders of magnitude from the smallest viruses (~17 nm) to the largest charismatic megafauna (blue whale, ~33 m).
Fig. 2: Spatial heterogeneity in the abundance of bacteria and VLPs may exist on extremely small scales in the oceans.
Fig. 3: The two main lifestyles of marine phages: lytic versus lysogenic.
Fig. 4: The marine food web, emphasizing the central role of the microbial loop and viral shunt in recycling DOM.
Fig. 5: Venn diagram showing cyanobacterial (left) and sulfur-oxidizing (right) cells.

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Acknowledgements

The authors thank D. Goldsmith, P. Salamon and C. Silveira for helpful discussions regarding the royal family model, and K. M. Scott for input regarding Fig. 5. M.B. was funded by grants DEB-1555854, IOS-1456301 and OCE-1722761 from the National Science Foundation. K.M. was supported by a National Science Foundation Graduate Research Fellowship (Award No. 3900101301). C.B. was supported by the Linton Tibbetts Endowed Graduate Student Fellowship. N.A.S. was supported by the Gulf Oceanographic Charitable Trust Endowed Fellowship.

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    Mya Breitbart, Chelsea Bonnain, Kema Malki & Natalie A. Sawaya

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Breitbart, M., Bonnain, C., Malki, K. et al. Phage puppet masters of the marine microbial realm. Nat Microbiol 3, 754–766 (2018). https://doi.org/10.1038/s41564-018-0166-y

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