TY - JOUR

T1 - Rethinking Phage Ecology by Rooting it Within an Established Plant Framework

AU - Clokie, Martha R.j.

AU - Blasdel, Bob G.

AU - Demars, Benoit O.l.

AU - Sicheritz-pontén, Thomas

PY - 2020

Y1 - 2020

N2 - Despite the abundance and significance of bacteriophages to microbial ecosystems, no broad ecological frameworks exist within which to determine “bacteriophage types” that reflect their ecological strategies and ways in which they interact with bacterial cells. To address this, we repurposed the well-established Grime's triangular CSR framework, which classifies plants according to three axes: competitiveness (C), ability to tolerate stress (S), and capacity to cope with disturbance (R). This framework is distinguished from other accepted schemes, as it seeks to identify individual characteristics of plants to understand their biological strategies and roles within an ecosystem. Our repurposing of the CSR triangle is based on phage transcription and the observation that typically phages have three major distinguishable transcription phases: early, middle, and late. We hypothesize that the proportion of genes expressed in these phases reflects key information about the phage “ecological strategy,” namely the C, S, and R strategies, allowing us to examine phages in a similar way to how plants are projected onto the triangle. In the “phage version” of this scheme, we suggest: (1) that some phages prioritize the early phase of transcription that shuts off host defense mechanisms, which reflects competitiveness; (2) other phages prioritize tuning resource management mechanisms in the cell such as nucleotide metabolism during their “mid” expression profile to tolerate stress; and (3) a further subset of phages (termed Ruderals) survive disturbance by investing significant resources into regeneration so they express a higher proportion of their genes during late infection. We examined 42 published phage transcriptomes and show that they fall into discrete CSR categories according to their expression profiles. We discuss these positions in the context of their biology, which is largely consistent with our predictions of specific phage characteristics. In this opinion article, we suggest a starting point to ascribe phages into different functional types and thus understand them in an ecological framework. We suggest that this may have far-reaching implications for the application of phages in therapy and their exploitation to manipulate bacterial communities. We invite further use of this framework via our online tool; www.PhageCSR.ml.

AB - Despite the abundance and significance of bacteriophages to microbial ecosystems, no broad ecological frameworks exist within which to determine “bacteriophage types” that reflect their ecological strategies and ways in which they interact with bacterial cells. To address this, we repurposed the well-established Grime's triangular CSR framework, which classifies plants according to three axes: competitiveness (C), ability to tolerate stress (S), and capacity to cope with disturbance (R). This framework is distinguished from other accepted schemes, as it seeks to identify individual characteristics of plants to understand their biological strategies and roles within an ecosystem. Our repurposing of the CSR triangle is based on phage transcription and the observation that typically phages have three major distinguishable transcription phases: early, middle, and late. We hypothesize that the proportion of genes expressed in these phases reflects key information about the phage “ecological strategy,” namely the C, S, and R strategies, allowing us to examine phages in a similar way to how plants are projected onto the triangle. In the “phage version” of this scheme, we suggest: (1) that some phages prioritize the early phase of transcription that shuts off host defense mechanisms, which reflects competitiveness; (2) other phages prioritize tuning resource management mechanisms in the cell such as nucleotide metabolism during their “mid” expression profile to tolerate stress; and (3) a further subset of phages (termed Ruderals) survive disturbance by investing significant resources into regeneration so they express a higher proportion of their genes during late infection. We examined 42 published phage transcriptomes and show that they fall into discrete CSR categories according to their expression profiles. We discuss these positions in the context of their biology, which is largely consistent with our predictions of specific phage characteristics. In this opinion article, we suggest a starting point to ascribe phages into different functional types and thus understand them in an ecological framework. We suggest that this may have far-reaching implications for the application of phages in therapy and their exploitation to manipulate bacterial communities. We invite further use of this framework via our online tool; www.PhageCSR.ml.

U2 - 10.1089/phage.2020.0015

DO - 10.1089/phage.2020.0015

M3 - Journal article

VL - 1

SP - 121

EP - 136

JO - PHAGE: Therapy, Applications, and Research

JF - PHAGE: Therapy, Applications, and Research

SN - 2641-6530

IS - 3

ER -