In bacteria-phage ecology and evolution, community context matters

Our understanding of the ecology and evolution of bacteria and their viruses, bacteriophages, in multispecies contexts is limited. A new review paper summarizes what little we know and highlights the many open questions that remain.

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This is a blog post about Blazanin, M., Turner, P.E. Community context matters for bacteria-phage ecology and evolution. ISME J (2021). https://doi.org/10.1038/s41396-021-01012-x

Bacteriophages, the viruses that infect bacterial cells, have been pivotal for some of the most foundational discoveries in biology, from the random nature of mutations, to DNA as genetic material and the triplet nature of the genetic code. During the last few decades, phages also have become important models of host-parasite interactions in ecology and evolutionary biology. In our new paper, we review the latest frontier of bacteria-phage experiments in ecology and evolution: multispecies communities.

Modern work with phages in multispecies communities build upon two distinct historical scientific foundations. Culture-based experiments investigated the ecological and coevolutionary dynamics of bacteria-phage pairs in the lab, while sequencing-based approaches observed bacteria and phages in their natural environments. These two approaches — reductionist culture-based experiments, and holistic culture-free observations — provided new insights into the interactions of bacteria and phages at the two extremes of community species richness: very simple, and very complex. However, these bodies of work left a key gap in the middle, limiting our ability to connect the findings of each to the other.

In our new paper, we review and synthesize the young and growing body of work seeking to fill that gap. These papers entail a wide variety of experiments with medium-complexity communities. We focus particularly on studies that manipulate community diversity, enabling us to directly measure how bacteria-phage dynamics shift in response to the presence of other bacterial species (“community context”). In total, we found just 9 papers that met the criteria of: (1) manipulating community context with at least 3 species, and (2) observing either the ecological or evolutionary dynamics of these systems. In our paper, we review the findings of these studies in two main categories: 1) the ecological effects of community context, and 2) the evolutionary effects of community context (Fig 1).

Figure 1. Conceptual overview of the effects of community context on bacteria-phage ecology and evolution. Community context can affect the ecology and evolution of bacteria and phages in numerous ways. Ecologically, other bacteria can suppress or elevate the density of the focal bacteria or phage population, or they can alter the ecological interaction between those two populations. Evolutionarily, community context can alter the rate and dynamics of host-phage evolution and coevolution, bias adaptation towards or away from some mechanisms, and interact with the pleiotropic consequences of evolution.

What we know

There was one clear trend for which nearly all the findings agreed: community context suppresses the density of both the focal phage, and the phage’s host bacteria. Such a finding is broadly consistent with expectations from ecological theory, but we also highlight how the degree of suppression is often stronger than expected, providing avenues for future work.

Where the experiments disagree

In contrast to the consistent ecological suppressive effect of community context, findings between studies diverged on a number of topics.

  • Experiments varied in how community context interacts with the ecological interaction between bacteria and phages. Findings ranged from community context amplifying the effect of phage on bacteria, dampening it, or even reversing it.
  • Studies found diverse ways that community context affects the nature, rate, and degree of coevolution between bacteria and phages. Again, findings ran the gamut, from having no effect to accelerating or decelerating evolutionary change
  • Papers reported a number of ways that community context interacted with the pleiotropic consequences of evolution in the focal bacteria or phages. Some found that community context did not interact with such trade-ups or trade-offs, while others documented clear evidence of community context altering the optimal phenotype along pleiotropic constraints or even changing the pleiotropic relationships themselves.

Where we don’t have enough data

Given the paucity of experiments, it’s not surprising that much remains unanswered about phages in medium-complexity multispecies communities. We highlighted a number of points with exciting potential for future research.

  • How does community context alter mechanisms of evolution? One study has shown that community context can alter the ways that bacteria evolve phage resistance, while another has shown how community context can provide new avenues for phage host-range expansion. Given the extremely diverse ways that bacteria and phages could evolve if locked in a never-ending arms race, we still don’t know how most of those adaptations are affected by community context
  • How do dynamics change as community diversity scales? Most of the experiments we found used relatively simple communities of 3-5 bacterial species, likely for experimental tractability. We still don’t know how both ecological and evolutionary patterns might shift in communities closer to natural levels of diversity.
  • How do dynamics change over longer periods of time? All of the experiments we discuss used timescales of just 10-15 generations, leaving it uncertain what would be observed over longer durations.

Concluding thoughts

In all, we concluded that the gap between simple experiments and multispecies observations of bacteria-phage systems remains large. We highlight in our paper the numerous questions unanswered by existing work, including the eventual goal of observing how ecology and evolution feedback on one another in multispecies communities with phages. Given the abundance of unknowns, experiments investigating bacteria-phage ecology and evolution in multispecies contexts will remain an exciting area for new research for many years to come.

Mike Blazanin

PhD Student, Yale University