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Published on: August 19, 2021
Suboptimal environmental conditions prolong phage epidemics in bacterial populations
Henry Goehlich1, Olivia Roth1,2, Michael Sieber3
1GEOMAR, Helmholtz Centre for Ocean Research, Marine Evolutionary Ecology, Kiel, Germany.
Abstract:
Infections by filamentous phages, which are usually nonlethal to the bacterial cells, influence bacterial fitness in various ways. While phage-encoded accessory genes, for example virulence genes, can be highly beneficial, the production of viral particles is energetically costly and often reduces bacterial growth. Consequently, if costs outweigh benefits, bacteria evolve resistance, which can shorten phage epidemics. Abiotic conditions are known to influence the net-fitness effect for infected bacteria. Their impact on the dynamics and trajectories of host resistance evolution, however, remains yet unknown. To address this, we experimentally evolved the bacterium Vibrio alginolyticus in the presence of a filamentous phage at three different salinity levels, that is (1) ambient, (2) 50% reduction and (3) fluctuations between reduced and ambient. In all three salinities, bacteria rapidly acquired resistance through super infection exclusion (SIE), whereby phage-infected cells acquired immunity at the cost of reduced growth. Over time, SIE was gradually replaced by evolutionary fitter surface receptor mutants (SRM). This replacement was significantly faster at ambient and fluctuating conditions compared with the low saline environment. Our experimentally parameterized mathematical model explains that suboptimal environmental conditions, in which bacterial growth is slower, slow down phage resistance evolution ultimately prolonging phage epidemics. Our results may explain the high prevalence of filamentous phages in natural environments where bacteria are frequently exposed to suboptimal conditions and constantly shifting selections regimes. Thus, our future ocean may favour the emergence of phage-born pathogenic bacteria and impose a greater risk for disease outbreaks, impacting not only marine animals but also humans.
Insights
Bacteria exposed to filamentous phages evolve resistance, but environmental conditions like salinity impact the speed of this evolution. Suboptimal conditions slow resistance, potentially prolonging phage epidemics and increasing disease risk.
Area of Science:
- Microbiology
- Evolutionary Biology
- Ecology
Background:
- Filamentous phages infect bacteria, impacting their fitness through costly viral particle production versus potential benefits from accessory genes.
- Bacterial resistance evolution to phages can shorten epidemics, but is influenced by abiotic factors.
- The effect of environmental conditions on the dynamics of host resistance evolution to phages is not well understood.
Purpose of the Study:
- To investigate how different salinity levels affect the evolution of bacterial resistance to filamentous phages.
- To determine the impact of environmental conditions on the rate and mechanisms of phage resistance evolution in bacteria.
- To model the relationship between environmental conditions, bacterial growth, and phage resistance evolution.
Main Methods:
- Experimental evolution of Vibrio alginolyticus in the presence of a filamentous phage under three salinity conditions: ambient, reduced, and fluctuating.
- Monitoring the emergence and replacement of resistance mechanisms: superinfection exclusion (SIE) and surface receptor mutants (SRM).
- Developing and parameterizing a mathematical model to explain observed evolutionary trajectories.
Main Results:
- Bacteria rapidly evolved resistance via SIE across all salinities, incurring a growth cost.
- SIE was gradually replaced by fitter surface receptor mutants (SRM), with replacement being faster under ambient and fluctuating salinities.
- Low salinity environments significantly slowed the evolution of fitter resistance mechanisms (SRM).
Conclusions:
- Suboptimal environmental conditions, such as low salinity, slow down bacterial phage resistance evolution, potentially prolonging phage epidemics.
- Environmental variability and suboptimal conditions may favor the persistence of phages in natural environments.
- Future ocean conditions could increase the risk of phage-born pathogenic bacteria, impacting marine ecosystems and human health.
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