Ecological determinants of altruism in prokaryote antivirus defense

TL;DR

The paper explores how prokaryotes choose between immune and programmed cell death strategies to defend against viruses, based on ecological factors like viral pressure and population size.

Contribution

The study identifies two key ecological determinants of optimal antivirus defense strategy in prokaryotes and validates these through mathematical modeling and comparative genomics.

Findings

As viral pressure increases, immunity becomes the preferred defense strategy.

Larger host populations favor programmed cell death (PCD) as the optimal defense strategy.

PCD can be maintained in unstructured populations over evolutionary timescales, even when it is not altruistic.

Abstract

Prokaryote evolution is driven in large part by the incessant arms race with viruses. Genomic investments in antivirus defense can be coarsely classified into two categories, immune systems that abrogate virus reproduction resulting in clearance, and programmed cell death (PCD) systems. Prokaryotic defense systems are enormously diverse, as revealed by an avalanche of recent discoveries, but the basic ecological determinants of defense strategy remain poorly understood. Through mathematical modeling of defense against lytic virus infection, we identify two principal determinants of optimal defense strategy and, through comparative genomics, we test this model by measuring the genomic investment into immunity vs. PCD among diverse bacteria and archaea. First, as viral pressure grows, immunity becomes the preferred defense strategy. Second, as host population size grows, PCD becomes the preferred strategy. We additionally predict that, although optimal strategy typically involves investment in both PCD and immunity, investment in immunity can also result in antagonism, increasing the likelihood that a PCD-competent cell will lyse due to infection. Together, these findings indicate that, generally, PCD is preferred at low multiplicity of infection (MOI) and immunity is preferred at high MOI. Finally, we demonstrate that PCD, which is typically considered to be an altruistic trait, is in some cases neutral and can be maintained in an unstructured population over an evolutionary timescale. Our work shows that the landscape of prokaryotic antivirus defense is substantially more complex than previously suspected.

The online version contains supplementary material available at 10.1186/s13062-025-00699-8.

Not applicable.

The online version contains supplementary material available at 10.1186/s13062-025-00699-8.

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