Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities

Abstract

Bacteria-phage coevolution, the reciprocal evolution between bacterial hosts and the phages that infect them, is an important driver of ecological and evolutionary processes in microbial communities. There is growing evidence from both laboratory and natural populations that coevolution can maintain phenotypic and genetic diversity, increase the rate of bacterial and phage evolution and divergence, affect community structure, and shape the evolution of ecologically relevant bacterial traits. Although the study of bacteria-phage coevolution is still in its infancy, with open questions regarding the specificity of the interaction, the gene networks of coevolving partners, and the relative importance of the coevolving interaction in complex communities and environments, there have recently been major advancements in the field. In this review, we sum up our current understanding of bacteria-phage coevolution both in the laboratory and in nature, discuss recent findings on both the coevolutionary process itself and the impact of coevolution on bacterial phenotype, diversity and interactions with other species (particularly their eukaryotic hosts), and outline future directions for the field.

Keywords: antagonistic; bacteriophage; host-parasite; infection; resistance; species interaction.

Fig 1

Diversity of phage reproductive strategies. (a) The ‘lytic’ phages replicate within their host cell and must burst the cell open to transmit to the next generation. These phages are therefore obligate killers of their hosts and are necessarily detrimental to host populations. (b) The ‘temperate’ phages (also referred to as ‘lysogenic’ phages or, once within the host genome, ‘prophages’) integrate into the host genome and reproduce along with the host cell. The integration of phage into the host genome can play a significant role in shaping bacterial phenotype and fitness (reviewed in Brüssow et al., 2004). (c) A relatively less common type of phage, the ‘filamentous’ phage, is able to reproduce without lysing the host cell and is continually secreted into the environment. These phages can also significantly alter bacterial phenotype, for example by encoding for toxins (Waldor & Mekalanos, 2012). Finally, the ‘cryptic prophages’ (not shown) are once temperate phages that have lost the ability to reproduce independently of their host (i.e. they can no longer enter the lytic cycle and transmit horizontally).

Fig 2

Illustration of bacterial resistance mechanisms against phages in the lytic cycle. There exist very few host-parasite systems for which the underlying mechanisms of infection and resistance are as well understood as bacteria–phage interactions, and yet new research continues to demonstrate the wide variety, complexity and sophistication of these coevolved systems (e.g. Høyland-Kroghsbo et al., 2013; Seed et al., 2013). Bacteria have evolved a number of defense mechanisms against invading phages, including those that (a) prevent phage adsorption, (b) degrade phage DNA inside the cell and/or block replication, and (c) initiate cell death upon infection. First, (a) bacteria can lose or alter the target receptor of phages, can produce an extracellular matrix of polysaccharides that blocks phage attachment, or can produce competitive inhibitors that bind to the phage attachment site. Phages can counter-adapt by altering their tail fiber attachment sites, by producing enzymes to degrade the matrix, or by changing the receptors to which they attach. (b) After successful phage attachment, bacteria can still prevent infection using a restriction-modification system, whereby recognized phage DNA is degraded by restriction enzymes, or through the CRISPR-Cas system, which has been identified in over 40% of bacteria and 90% of archaea (reviewed in Westra et al., 2012). (c) Finally, many bacterial species have mechanisms that lead to cell death, for example by degrading the cell wall, upon successful phage infection, thereby protecting neighboring cells from further infection. However, phages have been known to evolve mechanisms to evade even this level of defense by mimicking the host's defensive system (Blower et al., 2012).

Fig 3

An illustration of phage local adaptation across two populations. In the first case, (a) the bacteria–phage network across the two populations is nested, and the population containing phages with the broadest host range (in red) also contains the most resistant bacteria. This structure, which is loosely based on directional, arms-race selection, does not result in an overall pattern of local adaptation. In the second case, (b) the network remains nested, but phage host range and bacterial resistance are not correlated with population. Again, this structure does not result in an overall pattern of local adaptation. In the final case, (c) phages from one population are only infective to bacteria from the same population, although the network structure within each population remains nested. Unlike the others, this structure would lead to an overall pattern of phage local adaptation. Overall, we suggest that if phage-mediated selection typically leads to an increase in generalized resistance to phage attack, phages from one population should be most infective to hosts from populations under relaxed phage-mediated selection and least infective to those from populations under relatively strong phage-mediated selection, regardless of sympatry. Phage local adaptation therefore suggests both that hosts are unable to evolve resistance rapidly enough to escape their local phages and that phage infectivity/bacterial resistance is relatively specific.