Abstract
It is increasingly apparent that the dynamic microbial communities of long-lived hosts affect their phenotype, including resistance to disease. The host microbiota will change over time due to immigration of new species, interaction with the host immune system, and selection by bacteriophage viruses (phages), but the relative roles of each process are unclear. Previous metagenomic approaches confirm the presence of phages infecting host microbiota, and experimental coevolution of bacteria and phage populations in the laboratory has demonstrated rapid reciprocal change over time. The key challenge is to determine whether phages influence host-associated bacterial communities in nature, in the face of other selection pressures. I use a tree-bacteria-phage system to measure reciprocal changes in phage infectivity and bacterial resistance within microbial communities of tree hosts over one season. An experimental time shift shows that bacterial isolates are most resistant to lytic phages from the prior month and least resistant to those from the future month, providing clear evidence for both phage-mediated selection on bacterial communities and bacterial-mediated selection on phage communities in nature. These reciprocal changes suggest that phages indeed play a key role in shaping the microbiota of their eukaryotic hosts.
Highlights
Recent results from a natural bacteria-phage interaction within a long-lived eukaryotic host demonstrate that phages are highly prevalent within tree leaves and are locally adapted to bacterial hosts collected from the same host tree, relative to neighboring trees of the same species [12]
These lytic bacteriophages are obligate killers of their bacterial host cells and can impose strong selection on bacterial populations and communities for resistance [10]. This selection can lead to a temporary advantage for resistant bacterial mutants and/or immigrant bacterial strains that happen to be resistant to local phages, and it has great potential to maintain diversity at both the population and community levels [13,14,15]
Given the complexity of microbial communities in nature and the high dispersal rate of both bacteria and phages, it is unclear whether the dynamics observed in the lab are relevant to natural systems
Summary
In eight fully reciprocal crossinoculation experiments (one per tree), I measured both whether phage populations from a given time point were able to infect each of 24 bacteria from past, contemporary, and future time points (by measuring the presence of plaques—localized absence of bacterial growth—in which a given phage inoculum had been spotted onto a lawn of a given bacterial isolate) and how successful that phage inoculum was (the number of plaques formed). Because the observed decrease in bacterial resistance to phages from the future could be accounted for by changes in phage density or diversity over time, I examined the success of each phage inoculum on time-shifted bacterial hosts from past, present, and future time points.
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