Phage ecology and genetic exchange in soil

Abstract

The ecology of bacteriophages in soil is poorly understood with respect to the distribution, activity and life cycle of their hosts [29]. Perhaps the main reason for this is simply one of enumeration. Whilst it is relatively easy to detect a given phage if one knows its propagative host, it is not possible to observe those phages for which hosts are not known. It is estimated that at present only a small fraction of bacteria in soil can be cultivated and therefore the absolute numbers of bacteriophages within a soil sample remain hidden. Recent studies in aquatic systems have shown using direct counting procedures that the traditional phage assay may well underestimate phage numbers by as much as two orders of magnitude [15]. Studies on phage ecology are further complicated by the fact that their activity is dependent on the resources accessible to them, which, in the case of obligate parasites, are the availability of active hosts. In soil, microbial activity and abundance is discontinuous in space and time. Phage activity is dependent on this and must therefore mirror this by rapid replication in restricted growth periods and sites in order to maintain sufficient numbers of infective phages in the soil environment for the survival of the population. The concentration of active hosts in microsites may well increase the likelihood of phage-host encounters, at least in the short term. Unfortunately no information is available on the spatial distribution of bacteriophages in soil and it is likely that counts derived from a given mass of soil underestimate the concentration and significance in such sites. Phages may be involved in either lysogenic or virulent associations with their hosts in soil, however current detection procedures provide no indication of total numbers in the environment as these methods rely on the virulent reaction of the virus with its host. The importance of this point was illustrated by Reanney [18], who estimated that free phages of Bacillus stearothermophilus in soil, when detected by phage extraction and assay techniques, comprised only 20% of the population, the remainder being present as lysogens. Thus, even when working with a known host, the numbers of free phages infecting that host in a soil sample can only be taken as an indication of the total number of bacteriophages present. If it is true that 80% of temperate phages are present in soil as prophages, it perhaps serves as an indicator of how active bacteriophages actually occur in soil. Due to the hostile conditions that can prevail in the soil environment, the ability of a bacteriophage to lysogenise its host obviously confers a greater capacity to survive environmental stress such as: proteolytic enzymes, abiotic stress etc. If one considers the evolution of bacteriophages through the reshuffling of gene modules [16,21,22,23], then the lysogenic state must be one of the most important states for the interaction of different phage genomes and their subsequent recombination into new genomes in the environment.