In silico Evolution of Lysis-Lysogeny Strategies Reproduces Observed Lysogeny Propensities in Temperate Bacteriophages.

Vaibhhav Sinha,Akshit Goyal,Sine L Svenningsen,Sandeep Krishna,Szabolcs Semsey

doi:10.3389/fmicb.2017.01386

Abstract

Bacteriophages are the most abundant organisms on the planet and both lytic and temperate phages play key roles as shapers of ecosystems and drivers of bacterial evolution. Temperate phages can choose between (i) lysis: exploiting their bacterial hosts by producing multiple phage particles and releasing them by lysing the host cell, and (ii) lysogeny: establishing a potentially mutually beneficial relationship with the host by integrating their chromosome into the host cell's genome. Temperate phages exhibit lysogeny propensities in the curiously narrow range of 5–15%. For some temperate phages, the propensity is further regulated by the multiplicity of infection, such that single infections go predominantly lytic while multiple infections go predominantly lysogenic. We ask whether these observations can be explained by selection pressures in environments where multiple phage variants compete for the same host. Our models of pairwise competition, between phage variants that differ only in their propensity to lysogenize, predict the optimal lysogeny propensity to fall within the experimentally observed range. This prediction is robust to large variation in parameters such as the phage infection rate, burst size, decision rate, as well as bacterial growth rate, and initial phage to bacteria ratio. When we compete phage variants whose lysogeny strategies are allowed to depend upon multiplicity of infection, we find that the optimal strategy is one which switches from full lysis for single infections to full lysogeny for multiple infections. Previous attempts to explain lysogeny propensity have argued for bet-hedging that optimizes the response to fluctuating environmental conditions. Our results suggest that there is an additional selection pressure for lysogeny propensity within phage populations infecting a bacterial host, independent of environmental conditions.

Highlights

Temperate bacteriophages are crucial players in shaping ecosystems
We start the system described by Equations (1)–(4) with a small susceptible bacterial population, at a density B0(0) well below its carrying capacity, and we introduce the two phage variants in equal, but tiny, amounts Pi(0) [Default starting conditions: Pi(0)=10−4B0(0)]
The dynamics typically goes through three distinct stages (Figure 2): 1. The buildup: initially, uninfected bacteria grow exponentially, phages grow even faster, and lysogen numbers are another order of magnitude smaller

Summary

Introduction

Temperate bacteriophages are crucial players in shaping ecosystems. Recent studies have demonstrated that they play an important role in maintenance of diversity of bacterial communities (Bohannan and Lenski, 2000; Weinbauer and Rassoulzadegan, 2004), in the evolution and competitiveness of bacterial pathogens (Wagner and Waldor, 2002; Davies et al, 2016) and inIn silico Evolution of Lysis-Lysogeny in Temperate Bacteriophages acquisition of genetic material including antibiotic resistance genes (Balcazar, 2014; Shousa et al, 2015). Observations under laboratory conditions suggest that the lysogeny propensity lies in a narrow range, around 5 to 15%, for a wide range of temperate phage species (Hong et al, 1971; Kourilsky, 1973; Ikeuchi and Kurahashi, 1978; Schubert et al, 2007; Maynard et al, 2010; Broussard et al, 2013). Previous studies (Avlund et al, 2009b; Maslov and Sneppen, 2015) have attempted to explain the observed lysogeny propensity as the result of bet hedging in an uncertain environment In this scenario, lysogeny propensity reflects the relative likelihood of catastrophes that would destroy free phages or lysogens, and a narrow range of values would require a narrow range of likelihoods for such catastrophes

Methods

Results

Conclusion