Molecular Insights into Bacteriophage Evolution toward Its Host

Bacteriophages (phages), viruses that infect bacteria, are considered to be highly host-specific. To add to the knowledge about the evolution and development of bacteriophage speciation toward its host, we conducted a 21-day experiment with the broad host-range bacteriophage Aquamicrobium phage P14. We incubated the phage, which was previously isolated and enriched with the Alphaproteobacteria Aquamicrobium H14, with the Betaproteobacteria Alcaligenaceae H5. During the experiment, we observed an increase in the phage’s predation efficacy towards Alcaligenaceae H5. Furthermore, genome analysis and the comparison of the bacteriophage’s whole genome indicated that rather than being scattered evenly along the genome, mutations occur in specific regions. In total, 67% of the mutations with a frequency higher than 30% were located in genes that encode tail proteins, which are essential for host recognition and attachment. As control, we incubated the phage with the Alphaproteobacteria Aquamicrobium H8. In both experiments, most of the mutations appeared in the gene encoding the tail fiber protein. However, mutations in the gene encoding the tail tubular protein B were only observed when the phage was incubated with Alcaligenaceae H5. This highlights the phage’s tail as a key player in its adaptation to different hosts. We conclude that mutations in the phage’s genome were mainly located in tail-related regions. Further investigation is needed to fully characterize the adaptation mechanisms of the Aquamicrobium phage P14.

Alternative phage-host interaction in Lactococcus lactis: the carrier state drives rapid evolution of phages

Lactococcus lactis is a lactic acid bacterium widely used as starter culture for the manufacture of fermented milk products like quark, buttermilk and cheese. Bacteriophage infection of starter cultures is one of the biggest causes of fermentation failure and, therefore, lactococcal phages have received great attention from the scientific community in the past decades. In this work we present evidence for the establishment of a carrier state life cycle (CSLC) by a bacteriophage belonging to the c2 species, in the model laboratory strain L. lactis MG1363. Our results show that infection of L. lactis MG1363 with a second, dissimilar, c2 bacteriophage can induce the CSLC phage to enter an active lytic life cycle. The viral progeny obtained after this infection is a mixed population of phages with differences in their genome sequences and host ranges, indicative of an extremely rapid evolution process. We discuss the possible implications of this phage-host interaction, both with respect to bacteriophage evolution and phage adaptation to different hosts.IMPORTANCEOur results broaden the current know-how on the yet poorly investigated phage-host interaction mechanism of CSLC, propose a new bacteriophage evolution mechanism, and demonstrate that the outcome of phage infections is possibly more intricate than presently acknowledged.

A mathematical model of marine bacteriophage evolution

To explore how particularities of a host cell–virus system, and in particular host cell replication, affect viral evolution, in this paper we formulate a mathematical model of marine bacteriophage evolution. The intrinsic simplicity of real-life phage–bacteria systems, and in particular aquatic systems, for which the assumption of homogeneous mixing is well justified, allows for a reasonably simple model. The model constructed in this paper is based upon the Beretta–Kuang model of bacteria–phage interaction in an aquatic environment (Beretta & Kuang 1998 Math. Biosci. 149 , 57–76. ( doi:10.1016/S0025-5564(97)10015-3 )). Compared to the original Beretta–Kuang model, the model assumes the existence of a multitude of viral variants which correspond to continuously distributed phenotypes. It is noteworthy that the model is mechanistic (at least as far as the Beretta–Kuang model is mechanistic). Moreover, this model does not include any explicit law or mechanism of evolution; instead it is assumed, in agreement with the principles of Darwinian evolution, that evolution in this system can occur as a result of random mutations and natural selection. Simulations with a simplistic linear fitness landscape (which is chosen for the convenience of demonstration only and is not related to any real-life system) show that a pulse-type travelling wave moving towards increasing Darwinian fitness appears in the phenotype space. This implies that the overall fitness of a viral quasi-species steadily increases with time. That is, the simulations demonstrate that for an uneven fitness landscape random mutations combined with a mechanism of natural selection (for this particular system this is given by the conspecific competition for the resource) lead to the Darwinian evolution. It is noteworthy that in this system the speed of propagation of this wave (and hence the rate of evolution) is not constant but varies, depending on the current viral fitness and the abundance of susceptible bacteria. A specific feature of the original Beretta–Kuang model is that this model exhibits a supercritical Hopf bifurcation, leading to the loss of stability and the rise of self-sustained oscillations in the system. This phenomenon corresponds to the paradox of enrichment in the system. It is remarkable that under the conditions that ensure the bifurcation in the Beretta-Kuang model, the viral evolution model formulated in this paper also exhibits a rise in self-sustained oscillations of the abundance of all interacting populations. The propagation of the travelling wave, however, remains stable under these conditions. The only visible impact of the oscillations on viral evolution is a lower speed of the evolution.

Bacteriophages of Gordonia spp. Display a Spectrum of Diversity and Genetic Relationships

ABSTRACT The global bacteriophage population is large, dynamic, old, and highly diverse genetically. Many phages are tailed and contain double-stranded DNA, but these remain poorly characterized genomically. A collection of over 1,000 phages infecting Mycobacterium smegmatis reveals the diversity of phages of a common bacterial host, but their relationships to phages of phylogenetically proximal hosts are not known. Comparative sequence analysis of 79 phages isolated on Gordonia shows these also to be diverse and that the phages can be grouped into 14 clusters of related genomes, with an additional 14 phages that are “singletons” with no closely related genomes. One group of six phages is closely related to Cluster A mycobacteriophages, but the other Gordonia phages are distant relatives and share only 10% of their genes with the mycobacteriophages. The Gordonia phage genomes vary in genome length (17.1 to 103.4 kb), percentage of GC content (47 to 68.8%), and genome architecture and contain a variety of features not seen in other phage genomes. Like the mycobacteriophages, the highly mosaic Gordonia phages demonstrate a spectrum of genetic relationships. We show this is a general property of bacteriophages and suggest that any barriers to genetic exchange are soft and readily violable. IMPORTANCE Despite the numerical dominance of bacteriophages in the biosphere, there is a dearth of complete genomic sequences. Current genomic information reveals that phages are highly diverse genomically and have mosaic architectures formed by extensive horizontal genetic exchange. Comparative analysis of 79 phages of Gordonia shows them to not only be highly diverse, but to present a spectrum of relatedness. Most are distantly related to phages of the phylogenetically proximal host Mycobacterium smegmatis , although one group of Gordonia phages is more closely related to mycobacteriophages than to the other Gordonia phages. Phage genome sequence space remains largely unexplored, but further isolation and genomic comparison of phages targeted at related groups of hosts promise to reveal pathways of bacteriophage evolution.